diff --git a/beacon_node/beacon_chain/src/capella_readiness.rs b/beacon_node/beacon_chain/src/capella_readiness.rs
new file mode 100644
index 000000000..b15632105
--- /dev/null
+++ b/beacon_node/beacon_chain/src/capella_readiness.rs
@@ -0,0 +1,135 @@
+//! Provides tools for checking if a node is ready for the Capella upgrade and following merge
+//! transition.
+
+use crate::{BeaconChain, BeaconChainTypes};
+use execution_layer::http::{
+    ENGINE_FORKCHOICE_UPDATED_V2, ENGINE_GET_PAYLOAD_V2, ENGINE_NEW_PAYLOAD_V2,
+};
+use serde::{Deserialize, Serialize};
+use std::fmt;
+use std::time::Duration;
+use types::*;
+
+/// The time before the Capella fork when we will start issuing warnings about preparation.
+use super::merge_readiness::SECONDS_IN_A_WEEK;
+pub const CAPELLA_READINESS_PREPARATION_SECONDS: u64 = SECONDS_IN_A_WEEK * 2;
+pub const ENGINE_CAPABILITIES_REFRESH_INTERVAL: u64 = 300;
+
+#[derive(Debug, Serialize, Deserialize)]
+#[serde(rename_all = "snake_case")]
+#[serde(tag = "type")]
+pub enum CapellaReadiness {
+    /// The execution engine is capella-enabled (as far as we can tell)
+    Ready,
+    /// The EL can be reached and has the correct configuration, however it's not yet synced.
+    NotSynced,
+    /// We are connected to an execution engine which doesn't support the V2 engine api methods
+    V2MethodsNotSupported { error: String },
+    /// The transition configuration with the EL failed, there might be a problem with
+    /// connectivity, authentication or a difference in configuration.
+    ExchangeCapabilitiesFailed { error: String },
+    /// The user has not configured an execution endpoint
+    NoExecutionEndpoint,
+}
+
+impl fmt::Display for CapellaReadiness {
+    fn fmt(&self, f: &mut fmt::Formatter<'_>) -> fmt::Result {
+        match self {
+            CapellaReadiness::Ready => {
+                write!(f, "This node appears ready for Capella.")
+            }
+            CapellaReadiness::ExchangeCapabilitiesFailed { error } => write!(
+                f,
+                "Could not exchange capabilities with the \
+                    execution endpoint: {}",
+                error
+            ),
+            CapellaReadiness::NotSynced => write!(
+                f,
+                "The execution endpoint is connected and configured, \
+                    however it is not yet synced"
+            ),
+            CapellaReadiness::NoExecutionEndpoint => write!(
+                f,
+                "The --execution-endpoint flag is not specified, this is a \
+                    requirement post-merge"
+            ),
+            CapellaReadiness::V2MethodsNotSupported { error } => write!(
+                f,
+                "The execution endpoint does not appear to support \
+                    the required engine api methods for Capella: {}",
+                error
+            ),
+        }
+    }
+}
+
+impl<T: BeaconChainTypes> BeaconChain<T> {
+    /// Returns `true` if capella epoch is set and Capella fork has occurred or will
+    /// occur within `CAPELLA_READINESS_PREPARATION_SECONDS`
+    pub fn is_time_to_prepare_for_capella(&self, current_slot: Slot) -> bool {
+        if let Some(capella_epoch) = self.spec.capella_fork_epoch {
+            let capella_slot = capella_epoch.start_slot(T::EthSpec::slots_per_epoch());
+            let capella_readiness_preparation_slots =
+                CAPELLA_READINESS_PREPARATION_SECONDS / self.spec.seconds_per_slot;
+            // Return `true` if Capella has happened or is within the preparation time.
+            current_slot + capella_readiness_preparation_slots > capella_slot
+        } else {
+            // The Capella fork epoch has not been defined yet, no need to prepare.
+            false
+        }
+    }
+
+    /// Attempts to connect to the EL and confirm that it is ready for capella.
+    pub async fn check_capella_readiness(&self) -> CapellaReadiness {
+        if let Some(el) = self.execution_layer.as_ref() {
+            match el
+                .get_engine_capabilities(Some(Duration::from_secs(
+                    ENGINE_CAPABILITIES_REFRESH_INTERVAL,
+                )))
+                .await
+            {
+                Err(e) => {
+                    // The EL was either unreachable or responded with an error
+                    CapellaReadiness::ExchangeCapabilitiesFailed {
+                        error: format!("{:?}", e),
+                    }
+                }
+                Ok(capabilities) => {
+                    let mut missing_methods = String::from("Required Methods Unsupported:");
+                    let mut all_good = true;
+                    if !capabilities.get_payload_v2 {
+                        missing_methods.push(' ');
+                        missing_methods.push_str(ENGINE_GET_PAYLOAD_V2);
+                        all_good = false;
+                    }
+                    if !capabilities.forkchoice_updated_v2 {
+                        missing_methods.push(' ');
+                        missing_methods.push_str(ENGINE_FORKCHOICE_UPDATED_V2);
+                        all_good = false;
+                    }
+                    if !capabilities.new_payload_v2 {
+                        missing_methods.push(' ');
+                        missing_methods.push_str(ENGINE_NEW_PAYLOAD_V2);
+                        all_good = false;
+                    }
+
+                    if all_good {
+                        if !el.is_synced_for_notifier().await {
+                            // The EL is not synced.
+                            CapellaReadiness::NotSynced
+                        } else {
+                            CapellaReadiness::Ready
+                        }
+                    } else {
+                        CapellaReadiness::V2MethodsNotSupported {
+                            error: missing_methods,
+                        }
+                    }
+                }
+            }
+        } else {
+            CapellaReadiness::NoExecutionEndpoint
+        }
+    }
+}
diff --git a/beacon_node/beacon_chain/src/lib.rs b/beacon_node/beacon_chain/src/lib.rs
index c17b48517..2444c144f 100644
--- a/beacon_node/beacon_chain/src/lib.rs
+++ b/beacon_node/beacon_chain/src/lib.rs
@@ -11,6 +11,7 @@ mod block_times_cache;
 mod block_verification;
 pub mod builder;
 pub mod canonical_head;
+pub mod capella_readiness;
 pub mod chain_config;
 mod early_attester_cache;
 mod errors;
diff --git a/beacon_node/beacon_chain/src/merge_readiness.rs b/beacon_node/beacon_chain/src/merge_readiness.rs
index 4ef2102fd..c66df39ee 100644
--- a/beacon_node/beacon_chain/src/merge_readiness.rs
+++ b/beacon_node/beacon_chain/src/merge_readiness.rs
@@ -8,7 +8,7 @@ use std::fmt::Write;
 use types::*;
 
 /// The time before the Bellatrix fork when we will start issuing warnings about preparation.
-const SECONDS_IN_A_WEEK: u64 = 604800;
+pub const SECONDS_IN_A_WEEK: u64 = 604800;
 pub const MERGE_READINESS_PREPARATION_SECONDS: u64 = SECONDS_IN_A_WEEK * 2;
 
 #[derive(Default, Debug, Serialize, Deserialize)]
diff --git a/beacon_node/beacon_chain/src/test_utils.rs b/beacon_node/beacon_chain/src/test_utils.rs
index c5da51899..875ff845a 100644
--- a/beacon_node/beacon_chain/src/test_utils.rs
+++ b/beacon_node/beacon_chain/src/test_utils.rs
@@ -375,7 +375,6 @@ where
             .collect::<Result<_, _>>()
             .unwrap();
 
-        let spec = MainnetEthSpec::default_spec();
         let config = execution_layer::Config {
             execution_endpoints: urls,
             secret_files: vec![],
@@ -386,7 +385,6 @@ where
             config,
             self.runtime.task_executor.clone(),
             self.log.clone(),
-            &spec,
         )
         .unwrap();
 
diff --git a/beacon_node/client/src/builder.rs b/beacon_node/client/src/builder.rs
index b19b636c7..3b016ebda 100644
--- a/beacon_node/client/src/builder.rs
+++ b/beacon_node/client/src/builder.rs
@@ -154,7 +154,6 @@ where
                 config,
                 context.executor.clone(),
                 context.log().clone(),
-                &spec,
             )
             .map_err(|e| format!("unable to start execution layer endpoints: {:?}", e))?;
             Some(execution_layer)
diff --git a/beacon_node/client/src/notifier.rs b/beacon_node/client/src/notifier.rs
index 1da7a7970..c1d830bc0 100644
--- a/beacon_node/client/src/notifier.rs
+++ b/beacon_node/client/src/notifier.rs
@@ -1,5 +1,6 @@
 use crate::metrics;
 use beacon_chain::{
+    capella_readiness::CapellaReadiness,
     merge_readiness::{MergeConfig, MergeReadiness},
     BeaconChain, BeaconChainTypes, ExecutionStatus,
 };
@@ -313,6 +314,7 @@ pub fn spawn_notifier<T: BeaconChainTypes>(
 
             eth1_logging(&beacon_chain, &log);
             merge_readiness_logging(current_slot, &beacon_chain, &log).await;
+            capella_readiness_logging(current_slot, &beacon_chain, &log).await;
         }
     };
 
@@ -350,12 +352,15 @@ async fn merge_readiness_logging<T: BeaconChainTypes>(
     }
 
     if merge_completed && !has_execution_layer {
-        error!(
-            log,
-            "Execution endpoint required";
-            "info" => "you need an execution engine to validate blocks, see: \
-                       https://lighthouse-book.sigmaprime.io/merge-migration.html"
-        );
+        if !beacon_chain.is_time_to_prepare_for_capella(current_slot) {
+            // logging of the EE being offline is handled in `capella_readiness_logging()`
+            error!(
+                log,
+                "Execution endpoint required";
+                "info" => "you need an execution engine to validate blocks, see: \
+                           https://lighthouse-book.sigmaprime.io/merge-migration.html"
+            );
+        }
         return;
     }
 
@@ -419,6 +424,60 @@ async fn merge_readiness_logging<T: BeaconChainTypes>(
     }
 }
 
+/// Provides some helpful logging to users to indicate if their node is ready for Capella
+async fn capella_readiness_logging<T: BeaconChainTypes>(
+    current_slot: Slot,
+    beacon_chain: &BeaconChain<T>,
+    log: &Logger,
+) {
+    let capella_completed = beacon_chain
+        .canonical_head
+        .cached_head()
+        .snapshot
+        .beacon_block
+        .message()
+        .body()
+        .execution_payload()
+        .map_or(false, |payload| payload.withdrawals_root().is_ok());
+
+    let has_execution_layer = beacon_chain.execution_layer.is_some();
+
+    if capella_completed && has_execution_layer
+        || !beacon_chain.is_time_to_prepare_for_capella(current_slot)
+    {
+        return;
+    }
+
+    if capella_completed && !has_execution_layer {
+        error!(
+            log,
+            "Execution endpoint required";
+            "info" => "you need a Capella enabled execution engine to validate blocks, see: \
+                       https://lighthouse-book.sigmaprime.io/merge-migration.html"
+        );
+        return;
+    }
+
+    match beacon_chain.check_capella_readiness().await {
+        CapellaReadiness::Ready => {
+            info!(log, "Ready for Capella")
+        }
+        readiness @ CapellaReadiness::ExchangeCapabilitiesFailed { error: _ } => {
+            error!(
+                log,
+                "Not ready for Capella";
+                "info" => %readiness,
+                "hint" => "try updating Lighthouse and/or the execution layer",
+            )
+        }
+        readiness => warn!(
+            log,
+            "Not ready for Capella";
+            "info" => %readiness,
+        ),
+    }
+}
+
 fn eth1_logging<T: BeaconChainTypes>(beacon_chain: &BeaconChain<T>, log: &Logger) {
     let current_slot_opt = beacon_chain.slot().ok();
 
diff --git a/beacon_node/eth1/src/inner.rs b/beacon_node/eth1/src/inner.rs
index a44b31050..0468a02d2 100644
--- a/beacon_node/eth1/src/inner.rs
+++ b/beacon_node/eth1/src/inner.rs
@@ -122,7 +122,7 @@ impl SszEth1Cache {
                 cache: self.deposit_cache.to_deposit_cache()?,
                 last_processed_block: self.last_processed_block,
             }),
-            endpoint: endpoint_from_config(&config, &spec)
+            endpoint: endpoint_from_config(&config)
                 .map_err(|e| format!("Failed to create endpoint: {:?}", e))?,
             to_finalize: RwLock::new(None),
             // Set the remote head_block zero when creating a new instance. We only care about
diff --git a/beacon_node/eth1/src/service.rs b/beacon_node/eth1/src/service.rs
index 56c2411ba..31082394b 100644
--- a/beacon_node/eth1/src/service.rs
+++ b/beacon_node/eth1/src/service.rs
@@ -363,7 +363,7 @@ impl Default for Config {
     }
 }
 
-pub fn endpoint_from_config(config: &Config, spec: &ChainSpec) -> Result<HttpJsonRpc, String> {
+pub fn endpoint_from_config(config: &Config) -> Result<HttpJsonRpc, String> {
     match config.endpoint.clone() {
         Eth1Endpoint::Auth {
             endpoint,
@@ -373,16 +373,11 @@ pub fn endpoint_from_config(config: &Config, spec: &ChainSpec) -> Result<HttpJso
         } => {
             let auth = Auth::new_with_path(jwt_path, jwt_id, jwt_version)
                 .map_err(|e| format!("Failed to initialize jwt auth: {:?}", e))?;
-            HttpJsonRpc::new_with_auth(
-                endpoint,
-                auth,
-                Some(config.execution_timeout_multiplier),
-                spec,
-            )
-            .map_err(|e| format!("Failed to create eth1 json rpc client: {:?}", e))
+            HttpJsonRpc::new_with_auth(endpoint, auth, Some(config.execution_timeout_multiplier))
+                .map_err(|e| format!("Failed to create eth1 json rpc client: {:?}", e))
         }
         Eth1Endpoint::NoAuth(endpoint) => {
-            HttpJsonRpc::new(endpoint, Some(config.execution_timeout_multiplier), spec)
+            HttpJsonRpc::new(endpoint, Some(config.execution_timeout_multiplier))
                 .map_err(|e| format!("Failed to create eth1 json rpc client: {:?}", e))
         }
     }
@@ -409,7 +404,7 @@ impl Service {
                 deposit_cache: RwLock::new(DepositUpdater::new(
                     config.deposit_contract_deploy_block,
                 )),
-                endpoint: endpoint_from_config(&config, &spec)?,
+                endpoint: endpoint_from_config(&config)?,
                 to_finalize: RwLock::new(None),
                 remote_head_block: RwLock::new(None),
                 config: RwLock::new(config),
@@ -438,7 +433,7 @@ impl Service {
             inner: Arc::new(Inner {
                 block_cache: <_>::default(),
                 deposit_cache: RwLock::new(deposit_cache),
-                endpoint: endpoint_from_config(&config, &spec)
+                endpoint: endpoint_from_config(&config)
                     .map_err(Error::FailedToInitializeFromSnapshot)?,
                 to_finalize: RwLock::new(None),
                 remote_head_block: RwLock::new(None),
diff --git a/beacon_node/eth1/tests/test.rs b/beacon_node/eth1/tests/test.rs
index eb0d2371c..cd680478c 100644
--- a/beacon_node/eth1/tests/test.rs
+++ b/beacon_node/eth1/tests/test.rs
@@ -494,8 +494,7 @@ mod deposit_tree {
             let mut deposit_counts = vec![];
 
             let client =
-                HttpJsonRpc::new(SensitiveUrl::parse(&eth1.endpoint()).unwrap(), None, spec)
-                    .unwrap();
+                HttpJsonRpc::new(SensitiveUrl::parse(&eth1.endpoint()).unwrap(), None).unwrap();
 
             // Perform deposits to the smart contract, recording it's state along the way.
             for deposit in &deposits {
@@ -599,12 +598,8 @@ mod http {
                 .expect("should start eth1 environment");
             let deposit_contract = &eth1.deposit_contract;
             let web3 = eth1.web3();
-            let client = HttpJsonRpc::new(
-                SensitiveUrl::parse(&eth1.endpoint()).unwrap(),
-                None,
-                &MainnetEthSpec::default_spec(),
-            )
-            .unwrap();
+            let client =
+                HttpJsonRpc::new(SensitiveUrl::parse(&eth1.endpoint()).unwrap(), None).unwrap();
 
             let block_number = get_block_number(&web3).await;
             let logs = blocking_deposit_logs(&client, &eth1, 0..block_number).await;
@@ -720,8 +715,7 @@ mod fast {
             )
             .unwrap();
             let client =
-                HttpJsonRpc::new(SensitiveUrl::parse(&eth1.endpoint()).unwrap(), None, &spec)
-                    .unwrap();
+                HttpJsonRpc::new(SensitiveUrl::parse(&eth1.endpoint()).unwrap(), None).unwrap();
             let n = 10;
             let deposits: Vec<_> = (0..n).map(|_| random_deposit_data()).collect();
             for deposit in &deposits {
diff --git a/beacon_node/execution_layer/src/engine_api.rs b/beacon_node/execution_layer/src/engine_api.rs
index afc5cffe2..da5e991b0 100644
--- a/beacon_node/execution_layer/src/engine_api.rs
+++ b/beacon_node/execution_layer/src/engine_api.rs
@@ -1,4 +1,9 @@
 use crate::engines::ForkchoiceState;
+use crate::http::{
+    ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1, ENGINE_FORKCHOICE_UPDATED_V1,
+    ENGINE_FORKCHOICE_UPDATED_V2, ENGINE_GET_PAYLOAD_V1, ENGINE_GET_PAYLOAD_V2,
+    ENGINE_NEW_PAYLOAD_V1, ENGINE_NEW_PAYLOAD_V2,
+};
 pub use ethers_core::types::Transaction;
 use ethers_core::utils::rlp::{self, Decodable, Rlp};
 use http::deposit_methods::RpcError;
@@ -347,11 +352,8 @@ impl<T: EthSpec> GetPayloadResponse<T> {
     }
 }
 
-// This name is work in progress, it could
-// change when this method is actually proposed
-// but I'm writing this as it has been described
 #[derive(Clone, Copy, Debug)]
-pub struct SupportedApis {
+pub struct EngineCapabilities {
     pub new_payload_v1: bool,
     pub new_payload_v2: bool,
     pub forkchoice_updated_v1: bool,
@@ -360,3 +362,32 @@ pub struct SupportedApis {
     pub get_payload_v2: bool,
     pub exchange_transition_configuration_v1: bool,
 }
+
+impl EngineCapabilities {
+    pub fn to_response(&self) -> Vec<&str> {
+        let mut response = Vec::new();
+        if self.new_payload_v1 {
+            response.push(ENGINE_NEW_PAYLOAD_V1);
+        }
+        if self.new_payload_v2 {
+            response.push(ENGINE_NEW_PAYLOAD_V2);
+        }
+        if self.forkchoice_updated_v1 {
+            response.push(ENGINE_FORKCHOICE_UPDATED_V1);
+        }
+        if self.forkchoice_updated_v2 {
+            response.push(ENGINE_FORKCHOICE_UPDATED_V2);
+        }
+        if self.get_payload_v1 {
+            response.push(ENGINE_GET_PAYLOAD_V1);
+        }
+        if self.get_payload_v2 {
+            response.push(ENGINE_GET_PAYLOAD_V2);
+        }
+        if self.exchange_transition_configuration_v1 {
+            response.push(ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1);
+        }
+
+        response
+    }
+}
diff --git a/beacon_node/execution_layer/src/engine_api/http.rs b/beacon_node/execution_layer/src/engine_api/http.rs
index 60725192b..d1faab42c 100644
--- a/beacon_node/execution_layer/src/engine_api/http.rs
+++ b/beacon_node/execution_layer/src/engine_api/http.rs
@@ -7,10 +7,11 @@ use reqwest::header::CONTENT_TYPE;
 use sensitive_url::SensitiveUrl;
 use serde::de::DeserializeOwned;
 use serde_json::json;
-use tokio::sync::RwLock;
+use std::collections::HashSet;
+use tokio::sync::Mutex;
 
-use std::time::Duration;
-use types::{ChainSpec, EthSpec};
+use std::time::{Duration, SystemTime};
+use types::EthSpec;
 
 pub use deposit_log::{DepositLog, Log};
 pub use reqwest::Client;
@@ -48,8 +49,37 @@ pub const ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1: &str =
     "engine_exchangeTransitionConfigurationV1";
 pub const ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1_TIMEOUT: Duration = Duration::from_secs(1);
 
+pub const ENGINE_EXCHANGE_CAPABILITIES: &str = "engine_exchangeCapabilities";
+pub const ENGINE_EXCHANGE_CAPABILITIES_TIMEOUT: Duration = Duration::from_secs(1);
+
 /// This error is returned during a `chainId` call by Geth.
 pub const EIP155_ERROR_STR: &str = "chain not synced beyond EIP-155 replay-protection fork block";
+/// This code is returned by all clients when a method is not supported
+/// (verified geth, nethermind, erigon, besu)
+pub const METHOD_NOT_FOUND_CODE: i64 = -32601;
+
+pub static LIGHTHOUSE_CAPABILITIES: &[&str] = &[
+    ENGINE_NEW_PAYLOAD_V1,
+    ENGINE_NEW_PAYLOAD_V2,
+    ENGINE_GET_PAYLOAD_V1,
+    ENGINE_GET_PAYLOAD_V2,
+    ENGINE_FORKCHOICE_UPDATED_V1,
+    ENGINE_FORKCHOICE_UPDATED_V2,
+    ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1,
+];
+
+/// This is necessary because a user might run a capella-enabled version of
+/// lighthouse before they update to a capella-enabled execution engine.
+// TODO (mark): rip this out once we are post-capella on mainnet
+pub static PRE_CAPELLA_ENGINE_CAPABILITIES: EngineCapabilities = EngineCapabilities {
+    new_payload_v1: true,
+    new_payload_v2: false,
+    forkchoice_updated_v1: true,
+    forkchoice_updated_v2: false,
+    get_payload_v1: true,
+    get_payload_v2: false,
+    exchange_transition_configuration_v1: true,
+};
 
 /// Contains methods to convert arbitrary bytes to an ETH2 deposit contract object.
 pub mod deposit_log {
@@ -526,11 +556,47 @@ pub mod deposit_methods {
     }
 }
 
+#[derive(Clone, Debug)]
+pub struct CapabilitiesCacheEntry {
+    engine_capabilities: EngineCapabilities,
+    fetch_time: SystemTime,
+}
+
+impl CapabilitiesCacheEntry {
+    pub fn new(engine_capabilities: EngineCapabilities) -> Self {
+        Self {
+            engine_capabilities,
+            fetch_time: SystemTime::now(),
+        }
+    }
+
+    pub fn engine_capabilities(&self) -> &EngineCapabilities {
+        &self.engine_capabilities
+    }
+
+    pub fn age(&self) -> Duration {
+        // duration_since() may fail because measurements taken earlier
+        // are not guaranteed to always be before later measurements
+        // due to anomalies such as the system clock being adjusted
+        // either forwards or backwards
+        //
+        // In such cases, we'll just say the age is zero
+        SystemTime::now()
+            .duration_since(self.fetch_time)
+            .unwrap_or(Duration::ZERO)
+    }
+
+    /// returns `true` if the entry's age is >= age_limit
+    pub fn older_than(&self, age_limit: Option<Duration>) -> bool {
+        age_limit.map_or(false, |limit| self.age() >= limit)
+    }
+}
+
 pub struct HttpJsonRpc {
     pub client: Client,
     pub url: SensitiveUrl,
     pub execution_timeout_multiplier: u32,
-    pub cached_supported_apis: RwLock<Option<SupportedApis>>,
+    pub engine_capabilities_cache: Mutex<Option<CapabilitiesCacheEntry>>,
     auth: Option<Auth>,
 }
 
@@ -538,27 +604,12 @@ impl HttpJsonRpc {
     pub fn new(
         url: SensitiveUrl,
         execution_timeout_multiplier: Option<u32>,
-        spec: &ChainSpec,
     ) -> Result<Self, Error> {
-        // FIXME: remove this `cached_supported_apis` spec hack once the `engine_getCapabilities`
-        //        method is implemented in all execution clients:
-        //        https://github.com/ethereum/execution-apis/issues/321
-        let cached_supported_apis = RwLock::new(Some(SupportedApis {
-            new_payload_v1: true,
-            new_payload_v2: spec.capella_fork_epoch.is_some() || spec.eip4844_fork_epoch.is_some(),
-            forkchoice_updated_v1: true,
-            forkchoice_updated_v2: spec.capella_fork_epoch.is_some()
-                || spec.eip4844_fork_epoch.is_some(),
-            get_payload_v1: true,
-            get_payload_v2: spec.capella_fork_epoch.is_some() || spec.eip4844_fork_epoch.is_some(),
-            exchange_transition_configuration_v1: true,
-        }));
-
         Ok(Self {
             client: Client::builder().build()?,
             url,
             execution_timeout_multiplier: execution_timeout_multiplier.unwrap_or(1),
-            cached_supported_apis,
+            engine_capabilities_cache: Mutex::new(None),
             auth: None,
         })
     }
@@ -567,27 +618,12 @@ impl HttpJsonRpc {
         url: SensitiveUrl,
         auth: Auth,
         execution_timeout_multiplier: Option<u32>,
-        spec: &ChainSpec,
     ) -> Result<Self, Error> {
-        // FIXME: remove this `cached_supported_apis` spec hack once the `engine_getCapabilities`
-        //        method is implemented in all execution clients:
-        //        https://github.com/ethereum/execution-apis/issues/321
-        let cached_supported_apis = RwLock::new(Some(SupportedApis {
-            new_payload_v1: true,
-            new_payload_v2: spec.capella_fork_epoch.is_some() || spec.eip4844_fork_epoch.is_some(),
-            forkchoice_updated_v1: true,
-            forkchoice_updated_v2: spec.capella_fork_epoch.is_some()
-                || spec.eip4844_fork_epoch.is_some(),
-            get_payload_v1: true,
-            get_payload_v2: spec.capella_fork_epoch.is_some() || spec.eip4844_fork_epoch.is_some(),
-            exchange_transition_configuration_v1: true,
-        }));
-
         Ok(Self {
             client: Client::builder().build()?,
             url,
             execution_timeout_multiplier: execution_timeout_multiplier.unwrap_or(1),
-            cached_supported_apis,
+            engine_capabilities_cache: Mutex::new(None),
             auth: Some(auth),
         })
     }
@@ -893,35 +929,67 @@ impl HttpJsonRpc {
         Ok(response)
     }
 
-    // TODO: This is currently a stub for the `engine_getCapabilities`
-    //       method. This stub is unused because we set cached_supported_apis
-    //       in the constructor based on the `spec`
-    //       Implement this once the execution clients support it
-    //       https://github.com/ethereum/execution-apis/issues/321
-    pub async fn get_capabilities(&self) -> Result<SupportedApis, Error> {
-        Ok(SupportedApis {
-            new_payload_v1: true,
-            new_payload_v2: true,
-            forkchoice_updated_v1: true,
-            forkchoice_updated_v2: true,
-            get_payload_v1: true,
-            get_payload_v2: true,
-            exchange_transition_configuration_v1: true,
-        })
+    pub async fn exchange_capabilities(&self) -> Result<EngineCapabilities, Error> {
+        let params = json!([LIGHTHOUSE_CAPABILITIES]);
+
+        let response: Result<HashSet<String>, _> = self
+            .rpc_request(
+                ENGINE_EXCHANGE_CAPABILITIES,
+                params,
+                ENGINE_EXCHANGE_CAPABILITIES_TIMEOUT * self.execution_timeout_multiplier,
+            )
+            .await;
+
+        match response {
+            // TODO (mark): rip this out once we are post capella on mainnet
+            Err(error) => match error {
+                Error::ServerMessage { code, message: _ } if code == METHOD_NOT_FOUND_CODE => {
+                    Ok(PRE_CAPELLA_ENGINE_CAPABILITIES)
+                }
+                _ => Err(error),
+            },
+            Ok(capabilities) => Ok(EngineCapabilities {
+                new_payload_v1: capabilities.contains(ENGINE_NEW_PAYLOAD_V1),
+                new_payload_v2: capabilities.contains(ENGINE_NEW_PAYLOAD_V2),
+                forkchoice_updated_v1: capabilities.contains(ENGINE_FORKCHOICE_UPDATED_V1),
+                forkchoice_updated_v2: capabilities.contains(ENGINE_FORKCHOICE_UPDATED_V2),
+                get_payload_v1: capabilities.contains(ENGINE_GET_PAYLOAD_V1),
+                get_payload_v2: capabilities.contains(ENGINE_GET_PAYLOAD_V2),
+                exchange_transition_configuration_v1: capabilities
+                    .contains(ENGINE_EXCHANGE_TRANSITION_CONFIGURATION_V1),
+            }),
+        }
     }
 
-    pub async fn set_cached_supported_apis(&self, supported_apis: Option<SupportedApis>) {
-        *self.cached_supported_apis.write().await = supported_apis;
+    pub async fn clear_exchange_capabilties_cache(&self) {
+        *self.engine_capabilities_cache.lock().await = None;
     }
 
-    pub async fn get_cached_supported_apis(&self) -> Result<SupportedApis, Error> {
-        let cached_opt = *self.cached_supported_apis.read().await;
-        if let Some(supported_apis) = cached_opt {
-            Ok(supported_apis)
+    /// Returns the execution engine capabilities resulting from a call to
+    /// engine_exchangeCapabilities. If the capabilities cache is not populated,
+    /// or if it is populated with a cached result of age >= `age_limit`, this
+    /// method will fetch the result from the execution engine and populate the
+    /// cache before returning it. Otherwise it will return a cached result from
+    /// a previous call.
+    ///
+    /// Set `age_limit` to `None` to always return the cached result
+    /// Set `age_limit` to `Some(Duration::ZERO)` to force fetching from EE
+    pub async fn get_engine_capabilities(
+        &self,
+        age_limit: Option<Duration>,
+    ) -> Result<EngineCapabilities, Error> {
+        let mut lock = self.engine_capabilities_cache.lock().await;
+
+        if lock
+            .as_ref()
+            .map_or(true, |entry| entry.older_than(age_limit))
+        {
+            let engine_capabilities = self.exchange_capabilities().await?;
+            *lock = Some(CapabilitiesCacheEntry::new(engine_capabilities));
+            Ok(engine_capabilities)
         } else {
-            let supported_apis = self.get_capabilities().await?;
-            self.set_cached_supported_apis(Some(supported_apis)).await;
-            Ok(supported_apis)
+            // here entry is guaranteed to exist so unwrap() is safe
+            Ok(*lock.as_ref().unwrap().engine_capabilities())
         }
     }
 
@@ -931,10 +999,10 @@ impl HttpJsonRpc {
         &self,
         execution_payload: ExecutionPayload<T>,
     ) -> Result<PayloadStatusV1, Error> {
-        let supported_apis = self.get_cached_supported_apis().await?;
-        if supported_apis.new_payload_v2 {
+        let engine_capabilities = self.get_engine_capabilities(None).await?;
+        if engine_capabilities.new_payload_v2 {
             self.new_payload_v2(execution_payload).await
-        } else if supported_apis.new_payload_v1 {
+        } else if engine_capabilities.new_payload_v1 {
             self.new_payload_v1(execution_payload).await
         } else {
             Err(Error::RequiredMethodUnsupported("engine_newPayload"))
@@ -948,8 +1016,8 @@ impl HttpJsonRpc {
         fork_name: ForkName,
         payload_id: PayloadId,
     ) -> Result<ExecutionPayload<T>, Error> {
-        let supported_apis = self.get_cached_supported_apis().await?;
-        if supported_apis.get_payload_v2 {
+        let engine_capabilities = self.get_engine_capabilities(None).await?;
+        if engine_capabilities.get_payload_v2 {
             // TODO: modify this method to return GetPayloadResponse instead
             //       of throwing away the `block_value` and returning only the
             //       ExecutionPayload
@@ -957,7 +1025,7 @@ impl HttpJsonRpc {
                 .get_payload_v2(fork_name, payload_id)
                 .await?
                 .execution_payload())
-        } else if supported_apis.new_payload_v1 {
+        } else if engine_capabilities.new_payload_v1 {
             self.get_payload_v1(payload_id).await
         } else {
             Err(Error::RequiredMethodUnsupported("engine_getPayload"))
@@ -971,11 +1039,11 @@ impl HttpJsonRpc {
         forkchoice_state: ForkchoiceState,
         payload_attributes: Option<PayloadAttributes>,
     ) -> Result<ForkchoiceUpdatedResponse, Error> {
-        let supported_apis = self.get_cached_supported_apis().await?;
-        if supported_apis.forkchoice_updated_v2 {
+        let engine_capabilities = self.get_engine_capabilities(None).await?;
+        if engine_capabilities.forkchoice_updated_v2 {
             self.forkchoice_updated_v2(forkchoice_state, payload_attributes)
                 .await
-        } else if supported_apis.forkchoice_updated_v1 {
+        } else if engine_capabilities.forkchoice_updated_v1 {
             self.forkchoice_updated_v1(forkchoice_state, payload_attributes)
                 .await
         } else {
@@ -1003,7 +1071,6 @@ mod test {
     impl Tester {
         pub fn new(with_auth: bool) -> Self {
             let server = MockServer::unit_testing();
-            let spec = MainnetEthSpec::default_spec();
 
             let rpc_url = SensitiveUrl::parse(&server.url()).unwrap();
             let echo_url = SensitiveUrl::parse(&format!("{}/echo", server.url())).unwrap();
@@ -1014,13 +1081,13 @@ mod test {
                 let echo_auth =
                     Auth::new(JwtKey::from_slice(&DEFAULT_JWT_SECRET).unwrap(), None, None);
                 (
-                    Arc::new(HttpJsonRpc::new_with_auth(rpc_url, rpc_auth, None, &spec).unwrap()),
-                    Arc::new(HttpJsonRpc::new_with_auth(echo_url, echo_auth, None, &spec).unwrap()),
+                    Arc::new(HttpJsonRpc::new_with_auth(rpc_url, rpc_auth, None).unwrap()),
+                    Arc::new(HttpJsonRpc::new_with_auth(echo_url, echo_auth, None).unwrap()),
                 )
             } else {
                 (
-                    Arc::new(HttpJsonRpc::new(rpc_url, None, &spec).unwrap()),
-                    Arc::new(HttpJsonRpc::new(echo_url, None, &spec).unwrap()),
+                    Arc::new(HttpJsonRpc::new(rpc_url, None).unwrap()),
+                    Arc::new(HttpJsonRpc::new(echo_url, None).unwrap()),
                 )
             };
 
diff --git a/beacon_node/execution_layer/src/engines.rs b/beacon_node/execution_layer/src/engines.rs
index 271cca26c..5532fbb34 100644
--- a/beacon_node/execution_layer/src/engines.rs
+++ b/beacon_node/execution_layer/src/engines.rs
@@ -1,13 +1,15 @@
 //! Provides generic behaviour for multiple execution engines, specifically fallback behaviour.
 
 use crate::engine_api::{
-    Error as EngineApiError, ForkchoiceUpdatedResponse, PayloadAttributes, PayloadId,
+    EngineCapabilities, Error as EngineApiError, ForkchoiceUpdatedResponse, PayloadAttributes,
+    PayloadId,
 };
 use crate::HttpJsonRpc;
 use lru::LruCache;
-use slog::{debug, error, info, Logger};
+use slog::{debug, error, info, warn, Logger};
 use std::future::Future;
 use std::sync::Arc;
+use std::time::Duration;
 use task_executor::TaskExecutor;
 use tokio::sync::{watch, Mutex, RwLock};
 use tokio_stream::wrappers::WatchStream;
@@ -18,6 +20,7 @@ use types::ExecutionBlockHash;
 /// Since the size of each value is small (~100 bytes) a large number is used for safety.
 /// FIXME: check this assumption now that the key includes entire payload attributes which now includes withdrawals
 const PAYLOAD_ID_LRU_CACHE_SIZE: usize = 512;
+const CACHED_ENGINE_CAPABILITIES_AGE_LIMIT: Duration = Duration::from_secs(900); // 15 minutes
 
 /// Stores the remembered state of a engine.
 #[derive(Copy, Clone, PartialEq, Debug, Eq, Default)]
@@ -29,6 +32,14 @@ enum EngineStateInternal {
     AuthFailed,
 }
 
+#[derive(Copy, Clone, Debug, Default, Eq, PartialEq)]
+enum CapabilitiesCacheAction {
+    #[default]
+    None,
+    Update,
+    Clear,
+}
+
 /// A subset of the engine state to inform other services if the engine is online or offline.
 #[derive(Debug, Clone, PartialEq, Eq, Copy)]
 pub enum EngineState {
@@ -231,7 +242,7 @@ impl Engine {
     /// Run the `EngineApi::upcheck` function if the node's last known state is not synced. This
     /// might be used to recover the node if offline.
     pub async fn upcheck(&self) {
-        let state: EngineStateInternal = match self.api.upcheck().await {
+        let (state, cache_action) = match self.api.upcheck().await {
             Ok(()) => {
                 let mut state = self.state.write().await;
                 if **state != EngineStateInternal::Synced {
@@ -249,12 +260,12 @@ impl Engine {
                     );
                 }
                 state.update(EngineStateInternal::Synced);
-                **state
+                (**state, CapabilitiesCacheAction::Update)
             }
             Err(EngineApiError::IsSyncing) => {
                 let mut state = self.state.write().await;
                 state.update(EngineStateInternal::Syncing);
-                **state
+                (**state, CapabilitiesCacheAction::Update)
             }
             Err(EngineApiError::Auth(err)) => {
                 error!(
@@ -265,7 +276,7 @@ impl Engine {
 
                 let mut state = self.state.write().await;
                 state.update(EngineStateInternal::AuthFailed);
-                **state
+                (**state, CapabilitiesCacheAction::None)
             }
             Err(e) => {
                 error!(
@@ -276,10 +287,30 @@ impl Engine {
 
                 let mut state = self.state.write().await;
                 state.update(EngineStateInternal::Offline);
-                **state
+                // need to clear the engine capabilities cache if we detect the
+                // execution engine is offline as it is likely the engine is being
+                // updated to a newer version with new capabilities
+                (**state, CapabilitiesCacheAction::Clear)
             }
         };
 
+        // do this after dropping state lock guard to avoid holding two locks at once
+        match cache_action {
+            CapabilitiesCacheAction::None => {}
+            CapabilitiesCacheAction::Update => {
+                if let Err(e) = self
+                    .get_engine_capabilities(Some(CACHED_ENGINE_CAPABILITIES_AGE_LIMIT))
+                    .await
+                {
+                    warn!(self.log,
+                        "Error during exchange capabilities";
+                        "error" => ?e,
+                    )
+                }
+            }
+            CapabilitiesCacheAction::Clear => self.api.clear_exchange_capabilties_cache().await,
+        }
+
         debug!(
             self.log,
             "Execution engine upcheck complete";
@@ -287,6 +318,22 @@ impl Engine {
         );
     }
 
+    /// Returns the execution engine capabilities resulting from a call to
+    /// engine_exchangeCapabilities. If the capabilities cache is not populated,
+    /// or if it is populated with a cached result of age >= `age_limit`, this
+    /// method will fetch the result from the execution engine and populate the
+    /// cache before returning it. Otherwise it will return a cached result from
+    /// a previous call.
+    ///
+    /// Set `age_limit` to `None` to always return the cached result
+    /// Set `age_limit` to `Some(Duration::ZERO)` to force fetching from EE
+    pub async fn get_engine_capabilities(
+        &self,
+        age_limit: Option<Duration>,
+    ) -> Result<EngineCapabilities, EngineApiError> {
+        self.api.get_engine_capabilities(age_limit).await
+    }
+
     /// Run `func` on the node regardless of the node's current state.
     ///
     /// ## Note
diff --git a/beacon_node/execution_layer/src/lib.rs b/beacon_node/execution_layer/src/lib.rs
index 0a1a1eef3..ad72453f1 100644
--- a/beacon_node/execution_layer/src/lib.rs
+++ b/beacon_node/execution_layer/src/lib.rs
@@ -7,6 +7,7 @@
 use crate::payload_cache::PayloadCache;
 use auth::{strip_prefix, Auth, JwtKey};
 use builder_client::BuilderHttpClient;
+pub use engine_api::EngineCapabilities;
 use engine_api::Error as ApiError;
 pub use engine_api::*;
 pub use engine_api::{http, http::deposit_methods, http::HttpJsonRpc};
@@ -265,12 +266,7 @@ pub struct ExecutionLayer<T: EthSpec> {
 
 impl<T: EthSpec> ExecutionLayer<T> {
     /// Instantiate `Self` with an Execution engine specified in `Config`, using JSON-RPC via HTTP.
-    pub fn from_config(
-        config: Config,
-        executor: TaskExecutor,
-        log: Logger,
-        spec: &ChainSpec,
-    ) -> Result<Self, Error> {
+    pub fn from_config(config: Config, executor: TaskExecutor, log: Logger) -> Result<Self, Error> {
         let Config {
             execution_endpoints: urls,
             builder_url,
@@ -325,9 +321,8 @@ impl<T: EthSpec> ExecutionLayer<T> {
         let engine: Engine = {
             let auth = Auth::new(jwt_key, jwt_id, jwt_version);
             debug!(log, "Loaded execution endpoint"; "endpoint" => %execution_url, "jwt_path" => ?secret_file.as_path());
-            let api =
-                HttpJsonRpc::new_with_auth(execution_url, auth, execution_timeout_multiplier, spec)
-                    .map_err(Error::ApiError)?;
+            let api = HttpJsonRpc::new_with_auth(execution_url, auth, execution_timeout_multiplier)
+                .map_err(Error::ApiError)?;
             Engine::new(api, executor.clone(), &log)
         };
 
@@ -1367,6 +1362,26 @@ impl<T: EthSpec> ExecutionLayer<T> {
         }
     }
 
+    /// Returns the execution engine capabilities resulting from a call to
+    /// engine_exchangeCapabilities. If the capabilities cache is not populated,
+    /// or if it is populated with a cached result of age >= `age_limit`, this
+    /// method will fetch the result from the execution engine and populate the
+    /// cache before returning it. Otherwise it will return a cached result from
+    /// a previous call.
+    ///
+    /// Set `age_limit` to `None` to always return the cached result
+    /// Set `age_limit` to `Some(Duration::ZERO)` to force fetching from EE
+    pub async fn get_engine_capabilities(
+        &self,
+        age_limit: Option<Duration>,
+    ) -> Result<EngineCapabilities, Error> {
+        self.engine()
+            .request(|engine| engine.get_engine_capabilities(age_limit))
+            .await
+            .map_err(Box::new)
+            .map_err(Error::EngineError)
+    }
+
     /// Used during block production to determine if the merge has been triggered.
     ///
     /// ## Specification
diff --git a/beacon_node/execution_layer/src/test_utils/handle_rpc.rs b/beacon_node/execution_layer/src/test_utils/handle_rpc.rs
index 1e0963649..31a8a5da1 100644
--- a/beacon_node/execution_layer/src/test_utils/handle_rpc.rs
+++ b/beacon_node/execution_layer/src/test_utils/handle_rpc.rs
@@ -6,20 +6,27 @@ use serde_json::Value as JsonValue;
 use std::sync::Arc;
 use types::{EthSpec, ForkName};
 
+pub const GENERIC_ERROR_CODE: i64 = -1234;
+pub const BAD_PARAMS_ERROR_CODE: i64 = -32602;
+pub const UNKNOWN_PAYLOAD_ERROR_CODE: i64 = -38001;
+pub const FORK_REQUEST_MISMATCH_ERROR_CODE: i64 = -32000;
+
 pub async fn handle_rpc<T: EthSpec>(
     body: JsonValue,
     ctx: Arc<Context<T>>,
-) -> Result<JsonValue, String> {
+) -> Result<JsonValue, (String, i64)> {
     *ctx.previous_request.lock() = Some(body.clone());
 
     let method = body
         .get("method")
         .and_then(JsonValue::as_str)
-        .ok_or_else(|| "missing/invalid method field".to_string())?;
+        .ok_or_else(|| "missing/invalid method field".to_string())
+        .map_err(|s| (s, GENERIC_ERROR_CODE))?;
 
     let params = body
         .get("params")
-        .ok_or_else(|| "missing/invalid params field".to_string())?;
+        .ok_or_else(|| "missing/invalid params field".to_string())
+        .map_err(|s| (s, GENERIC_ERROR_CODE))?;
 
     match method {
         ETH_SYNCING => Ok(JsonValue::Bool(false)),
@@ -27,7 +34,8 @@ pub async fn handle_rpc<T: EthSpec>(
             let tag = params
                 .get(0)
                 .and_then(JsonValue::as_str)
-                .ok_or_else(|| "missing/invalid params[0] value".to_string())?;
+                .ok_or_else(|| "missing/invalid params[0] value".to_string())
+                .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
 
             match tag {
                 "latest" => Ok(serde_json::to_value(
@@ -36,7 +44,10 @@ pub async fn handle_rpc<T: EthSpec>(
                         .latest_execution_block(),
                 )
                 .unwrap()),
-                other => Err(format!("The tag {} is not supported", other)),
+                other => Err((
+                    format!("The tag {} is not supported", other),
+                    BAD_PARAMS_ERROR_CODE,
+                )),
             }
         }
         ETH_GET_BLOCK_BY_HASH => {
@@ -47,7 +58,8 @@ pub async fn handle_rpc<T: EthSpec>(
                 .and_then(|s| {
                     s.parse()
                         .map_err(|e| format!("unable to parse hash: {:?}", e))
-                })?;
+                })
+                .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
 
             // If we have a static response set, just return that.
             if let Some(response) = *ctx.static_get_block_by_hash_response.lock() {
@@ -57,7 +69,8 @@ pub async fn handle_rpc<T: EthSpec>(
             let full_tx = params
                 .get(1)
                 .and_then(JsonValue::as_bool)
-                .ok_or_else(|| "missing/invalid params[1] value".to_string())?;
+                .ok_or_else(|| "missing/invalid params[1] value".to_string())
+                .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
             if full_tx {
                 Ok(serde_json::to_value(
                     ctx.execution_block_generator
@@ -76,15 +89,17 @@ pub async fn handle_rpc<T: EthSpec>(
         }
         ENGINE_NEW_PAYLOAD_V1 | ENGINE_NEW_PAYLOAD_V2 => {
             let request = match method {
-                ENGINE_NEW_PAYLOAD_V1 => {
-                    JsonExecutionPayload::V1(get_param::<JsonExecutionPayloadV1<T>>(params, 0)?)
-                }
+                ENGINE_NEW_PAYLOAD_V1 => JsonExecutionPayload::V1(
+                    get_param::<JsonExecutionPayloadV1<T>>(params, 0)
+                        .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?,
+                ),
                 ENGINE_NEW_PAYLOAD_V2 => get_param::<JsonExecutionPayloadV2<T>>(params, 0)
                     .map(|jep| JsonExecutionPayload::V2(jep))
                     .or_else(|_| {
                         get_param::<JsonExecutionPayloadV1<T>>(params, 0)
                             .map(|jep| JsonExecutionPayload::V1(jep))
-                    })?,
+                    })
+                    .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?,
                 // TODO(4844) add that here..
                 _ => unreachable!(),
             };
@@ -97,20 +112,29 @@ pub async fn handle_rpc<T: EthSpec>(
             match fork {
                 ForkName::Merge => {
                     if matches!(request, JsonExecutionPayload::V2(_)) {
-                        return Err(format!(
-                            "{} called with `ExecutionPayloadV2` before capella fork!",
-                            method
+                        return Err((
+                            format!(
+                                "{} called with `ExecutionPayloadV2` before Capella fork!",
+                                method
+                            ),
+                            GENERIC_ERROR_CODE,
                         ));
                     }
                 }
                 ForkName::Capella => {
                     if method == ENGINE_NEW_PAYLOAD_V1 {
-                        return Err(format!("{} called after capella fork!", method));
+                        return Err((
+                            format!("{} called after Capella fork!", method),
+                            GENERIC_ERROR_CODE,
+                        ));
                     }
                     if matches!(request, JsonExecutionPayload::V1(_)) {
-                        return Err(format!(
-                            "{} called with `ExecutionPayloadV1` after capella fork!",
-                            method
+                        return Err((
+                            format!(
+                                "{} called with `ExecutionPayloadV1` after Capella fork!",
+                                method
+                            ),
+                            GENERIC_ERROR_CODE,
                         ));
                     }
                 }
@@ -149,14 +173,20 @@ pub async fn handle_rpc<T: EthSpec>(
             Ok(serde_json::to_value(JsonPayloadStatusV1::from(response)).unwrap())
         }
         ENGINE_GET_PAYLOAD_V1 | ENGINE_GET_PAYLOAD_V2 => {
-            let request: JsonPayloadIdRequest = get_param(params, 0)?;
+            let request: JsonPayloadIdRequest =
+                get_param(params, 0).map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
             let id = request.into();
 
             let response = ctx
                 .execution_block_generator
                 .write()
                 .get_payload(&id)
-                .ok_or_else(|| format!("no payload for id {:?}", id))?;
+                .ok_or_else(|| {
+                    (
+                        format!("no payload for id {:?}", id),
+                        UNKNOWN_PAYLOAD_ERROR_CODE,
+                    )
+                })?;
 
             // validate method called correctly according to shanghai fork time
             if ctx
@@ -166,7 +196,10 @@ pub async fn handle_rpc<T: EthSpec>(
                 == ForkName::Capella
                 && method == ENGINE_GET_PAYLOAD_V1
             {
-                return Err(format!("{} called after capella fork!", method));
+                return Err((
+                    format!("{} called after Capella fork!", method),
+                    FORK_REQUEST_MISMATCH_ERROR_CODE,
+                ));
             }
             // TODO(4844) add 4844 error checking here
 
@@ -195,38 +228,42 @@ pub async fn handle_rpc<T: EthSpec>(
             }
         }
         ENGINE_FORKCHOICE_UPDATED_V1 | ENGINE_FORKCHOICE_UPDATED_V2 => {
-            let forkchoice_state: JsonForkchoiceStateV1 = get_param(params, 0)?;
+            let forkchoice_state: JsonForkchoiceStateV1 =
+                get_param(params, 0).map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
             let payload_attributes = match method {
                 ENGINE_FORKCHOICE_UPDATED_V1 => {
-                    let jpa1: Option<JsonPayloadAttributesV1> = get_param(params, 1)?;
+                    let jpa1: Option<JsonPayloadAttributesV1> =
+                        get_param(params, 1).map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?;
                     jpa1.map(JsonPayloadAttributes::V1)
                 }
                 ENGINE_FORKCHOICE_UPDATED_V2 => {
                     // we can't use `deny_unknown_fields` without breaking compatibility with some
                     // clients that haven't updated to the latest engine_api spec. So instead we'll
                     // need to deserialize based on timestamp
-                    get_param::<Option<JsonPayloadAttributes>>(params, 1).and_then(|pa| {
-                        pa.and_then(|pa| {
-                            match ctx
-                                .execution_block_generator
-                                .read()
-                                .get_fork_at_timestamp(*pa.timestamp())
-                            {
-                                ForkName::Merge => {
-                                    get_param::<Option<JsonPayloadAttributesV1>>(params, 1)
-                                        .map(|opt| opt.map(JsonPayloadAttributes::V1))
-                                        .transpose()
+                    get_param::<Option<JsonPayloadAttributes>>(params, 1)
+                        .and_then(|pa| {
+                            pa.and_then(|pa| {
+                                match ctx
+                                    .execution_block_generator
+                                    .read()
+                                    .get_fork_at_timestamp(*pa.timestamp())
+                                {
+                                    ForkName::Merge => {
+                                        get_param::<Option<JsonPayloadAttributesV1>>(params, 1)
+                                            .map(|opt| opt.map(JsonPayloadAttributes::V1))
+                                            .transpose()
+                                    }
+                                    ForkName::Capella => {
+                                        get_param::<Option<JsonPayloadAttributesV2>>(params, 1)
+                                            .map(|opt| opt.map(JsonPayloadAttributes::V2))
+                                            .transpose()
+                                    }
+                                    _ => unreachable!(),
                                 }
-                                ForkName::Capella => {
-                                    get_param::<Option<JsonPayloadAttributesV2>>(params, 1)
-                                        .map(|opt| opt.map(JsonPayloadAttributes::V2))
-                                        .transpose()
-                                }
-                                _ => unreachable!(),
-                            }
+                            })
+                            .transpose()
                         })
-                        .transpose()
-                    })?
+                        .map_err(|s| (s, BAD_PARAMS_ERROR_CODE))?
                 }
                 _ => unreachable!(),
             };
@@ -240,20 +277,29 @@ pub async fn handle_rpc<T: EthSpec>(
                 {
                     ForkName::Merge => {
                         if matches!(pa, JsonPayloadAttributes::V2(_)) {
-                            return Err(format!(
-                                "{} called with `JsonPayloadAttributesV2` before capella fork!",
-                                method
+                            return Err((
+                                format!(
+                                    "{} called with `JsonPayloadAttributesV2` before Capella fork!",
+                                    method
+                                ),
+                                GENERIC_ERROR_CODE,
                             ));
                         }
                     }
                     ForkName::Capella => {
                         if method == ENGINE_FORKCHOICE_UPDATED_V1 {
-                            return Err(format!("{} called after capella fork!", method));
+                            return Err((
+                                format!("{} called after Capella fork!", method),
+                                FORK_REQUEST_MISMATCH_ERROR_CODE,
+                            ));
                         }
                         if matches!(pa, JsonPayloadAttributes::V1(_)) {
-                            return Err(format!(
-                                "{} called with `JsonPayloadAttributesV1` after capella fork!",
-                                method
+                            return Err((
+                                format!(
+                                    "{} called with `JsonPayloadAttributesV1` after Capella fork!",
+                                    method
+                                ),
+                                FORK_REQUEST_MISMATCH_ERROR_CODE,
                             ));
                         }
                     }
@@ -281,10 +327,14 @@ pub async fn handle_rpc<T: EthSpec>(
                 return Ok(serde_json::to_value(response).unwrap());
             }
 
-            let mut response = ctx.execution_block_generator.write().forkchoice_updated(
-                forkchoice_state.into(),
-                payload_attributes.map(|json| json.into()),
-            )?;
+            let mut response = ctx
+                .execution_block_generator
+                .write()
+                .forkchoice_updated(
+                    forkchoice_state.into(),
+                    payload_attributes.map(|json| json.into()),
+                )
+                .map_err(|s| (s, GENERIC_ERROR_CODE))?;
 
             if let Some(mut status) = ctx.static_forkchoice_updated_response.lock().clone() {
                 if status.status == PayloadStatusV1Status::Valid {
@@ -305,9 +355,13 @@ pub async fn handle_rpc<T: EthSpec>(
             };
             Ok(serde_json::to_value(transition_config).unwrap())
         }
-        other => Err(format!(
-            "The method {} does not exist/is not available",
-            other
+        ENGINE_EXCHANGE_CAPABILITIES => {
+            let engine_capabilities = ctx.engine_capabilities.read();
+            Ok(serde_json::to_value(engine_capabilities.to_response()).unwrap())
+        }
+        other => Err((
+            format!("The method {} does not exist/is not available", other),
+            METHOD_NOT_FOUND_CODE,
         )),
     }
 }
diff --git a/beacon_node/execution_layer/src/test_utils/mock_builder.rs b/beacon_node/execution_layer/src/test_utils/mock_builder.rs
index 8ce4a6556..06b5e81eb 100644
--- a/beacon_node/execution_layer/src/test_utils/mock_builder.rs
+++ b/beacon_node/execution_layer/src/test_utils/mock_builder.rs
@@ -84,8 +84,7 @@ impl<E: EthSpec> TestingBuilder<E> {
         };
 
         let el =
-            ExecutionLayer::from_config(config, executor.clone(), executor.log().clone(), &spec)
-                .unwrap();
+            ExecutionLayer::from_config(config, executor.clone(), executor.log().clone()).unwrap();
 
         // This should probably be done for all fields, we only update ones we are testing with so far.
         let mut context = Context::for_mainnet();
diff --git a/beacon_node/execution_layer/src/test_utils/mock_execution_layer.rs b/beacon_node/execution_layer/src/test_utils/mock_execution_layer.rs
index d061f13a6..ad73b2b4e 100644
--- a/beacon_node/execution_layer/src/test_utils/mock_execution_layer.rs
+++ b/beacon_node/execution_layer/src/test_utils/mock_execution_layer.rs
@@ -73,8 +73,7 @@ impl<T: EthSpec> MockExecutionLayer<T> {
             ..Default::default()
         };
         let el =
-            ExecutionLayer::from_config(config, executor.clone(), executor.log().clone(), &spec)
-                .unwrap();
+            ExecutionLayer::from_config(config, executor.clone(), executor.log().clone()).unwrap();
 
         Self {
             server,
@@ -106,7 +105,7 @@ impl<T: EthSpec> MockExecutionLayer<T> {
             prev_randao,
             Address::repeat_byte(42),
             // FIXME: think about how to handle different forks / withdrawals here..
-            Some(vec![]),
+            None,
         );
 
         // Insert a proposer to ensure the fork choice updated command works.
diff --git a/beacon_node/execution_layer/src/test_utils/mod.rs b/beacon_node/execution_layer/src/test_utils/mod.rs
index bad02e369..adf9358f0 100644
--- a/beacon_node/execution_layer/src/test_utils/mod.rs
+++ b/beacon_node/execution_layer/src/test_utils/mod.rs
@@ -22,6 +22,7 @@ use tokio::{runtime, sync::oneshot};
 use types::{EthSpec, ExecutionBlockHash, Uint256};
 use warp::{http::StatusCode, Filter, Rejection};
 
+use crate::EngineCapabilities;
 pub use execution_block_generator::{generate_pow_block, Block, ExecutionBlockGenerator};
 pub use hook::Hook;
 pub use mock_builder::{Context as MockBuilderContext, MockBuilder, Operation, TestingBuilder};
@@ -31,6 +32,15 @@ pub const DEFAULT_TERMINAL_DIFFICULTY: u64 = 6400;
 pub const DEFAULT_TERMINAL_BLOCK: u64 = 64;
 pub const DEFAULT_JWT_SECRET: [u8; 32] = [42; 32];
 pub const DEFAULT_BUILDER_THRESHOLD_WEI: u128 = 1_000_000_000_000_000_000;
+pub const DEFAULT_ENGINE_CAPABILITIES: EngineCapabilities = EngineCapabilities {
+    new_payload_v1: true,
+    new_payload_v2: true,
+    forkchoice_updated_v1: true,
+    forkchoice_updated_v2: true,
+    get_payload_v1: true,
+    get_payload_v2: true,
+    exchange_transition_configuration_v1: true,
+};
 
 mod execution_block_generator;
 mod handle_rpc;
@@ -117,6 +127,7 @@ impl<T: EthSpec> MockServer<T> {
             hook: <_>::default(),
             new_payload_statuses: <_>::default(),
             fcu_payload_statuses: <_>::default(),
+            engine_capabilities: Arc::new(RwLock::new(DEFAULT_ENGINE_CAPABILITIES)),
             _phantom: PhantomData,
         });
 
@@ -147,6 +158,10 @@ impl<T: EthSpec> MockServer<T> {
         }
     }
 
+    pub fn set_engine_capabilities(&self, engine_capabilities: EngineCapabilities) {
+        *self.ctx.engine_capabilities.write() = engine_capabilities;
+    }
+
     pub fn new(
         handle: &runtime::Handle,
         jwt_key: JwtKey,
@@ -469,6 +484,7 @@ pub struct Context<T: EthSpec> {
     pub new_payload_statuses: Arc<Mutex<HashMap<ExecutionBlockHash, PayloadStatusV1>>>,
     pub fcu_payload_statuses: Arc<Mutex<HashMap<ExecutionBlockHash, PayloadStatusV1>>>,
 
+    pub engine_capabilities: Arc<RwLock<EngineCapabilities>>,
     pub _phantom: PhantomData<T>,
 }
 
@@ -620,11 +636,11 @@ pub fn serve<T: EthSpec>(
                         "jsonrpc": JSONRPC_VERSION,
                         "result": result
                     }),
-                    Err(message) => json!({
+                    Err((message, code)) => json!({
                         "id": id,
                         "jsonrpc": JSONRPC_VERSION,
                         "error": {
-                            "code": -1234,   // Junk error code.
+                            "code": code,
                             "message": message
                         }
                     }),
diff --git a/testing/execution_engine_integration/src/test_rig.rs b/testing/execution_engine_integration/src/test_rig.rs
index 2daacb0ad..fe7e51e92 100644
--- a/testing/execution_engine_integration/src/test_rig.rs
+++ b/testing/execution_engine_integration/src/test_rig.rs
@@ -127,7 +127,7 @@ impl<E: GenericExecutionEngine> TestRig<E> {
                 ..Default::default()
             };
             let execution_layer =
-                ExecutionLayer::from_config(config, executor.clone(), log.clone(), &spec).unwrap();
+                ExecutionLayer::from_config(config, executor.clone(), log.clone()).unwrap();
             ExecutionPair {
                 execution_engine,
                 execution_layer,
@@ -146,7 +146,7 @@ impl<E: GenericExecutionEngine> TestRig<E> {
                 ..Default::default()
             };
             let execution_layer =
-                ExecutionLayer::from_config(config, executor, log.clone(), &spec).unwrap();
+                ExecutionLayer::from_config(config, executor, log.clone()).unwrap();
             ExecutionPair {
                 execution_engine,
                 execution_layer,