diff --git a/CHANGELOG.md b/CHANGELOG.md
index f8a523e85d..423b364e74 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -40,6 +40,10 @@ Ref: https://keepachangelog.com/en/1.0.0/
 
 Every module contains its own CHANGELOG.md. Please refer to the module you are interested in.
 
+### Improvements
+
+* (genutil) [#21701](https://github.com/cosmos/cosmos-sdk/pull/21701) Improved error messages for genesis validation.
+
 ## [v0.52.0](https://github.com/cosmos/cosmos-sdk/releases/tag/v0.52.0) - 2024-XX-XX
 
 Every module contains its own CHANGELOG.md. Please refer to the module you are interested in.
diff --git a/x/genutil/client/cli/validate_genesis.go b/x/genutil/client/cli/validate_genesis.go
index bc22ebda51..49c16054cc 100644
--- a/x/genutil/client/cli/validate_genesis.go
+++ b/x/genutil/client/cli/validate_genesis.go
@@ -2,7 +2,10 @@ package cli
 
 import (
 	"encoding/json"
+	"errors"
 	"fmt"
+	"io"
+	"strings"
 
 	"github.com/spf13/cobra"
 
@@ -32,7 +35,7 @@ func ValidateGenesisCmd(genMM genesisMM) *cobra.Command {
 
 			appGenesis, err := types.AppGenesisFromFile(genesis)
 			if err != nil {
-				return err
+				return enrichUnmarshalError(err)
 			}
 
 			if err := appGenesis.ValidateAndComplete(); err != nil {
@@ -41,12 +44,19 @@ func ValidateGenesisCmd(genMM genesisMM) *cobra.Command {
 
 			var genState map[string]json.RawMessage
 			if err = json.Unmarshal(appGenesis.AppState, &genState); err != nil {
+				if strings.Contains(err.Error(), "unexpected end of JSON input") {
+					return fmt.Errorf("app_state is missing in the genesis file: %s", err.Error())
+				}
 				return fmt.Errorf("error unmarshalling genesis doc %s: %w", genesis, err)
 			}
 
 			if genMM != nil {
 				if err = genMM.ValidateGenesis(genState); err != nil {
-					return fmt.Errorf("error validating genesis file %s: %w", genesis, err)
+					errStr := fmt.Sprintf("error validating genesis file %s: %s", genesis, err.Error())
+					if errors.Is(err, io.EOF) {
+						errStr = fmt.Sprintf("%s: section is missing in the app_state", errStr)
+					}
+					return fmt.Errorf("%s", errStr)
 				}
 			}
 
@@ -55,3 +65,11 @@ func ValidateGenesisCmd(genMM genesisMM) *cobra.Command {
 		},
 	}
 }
+
+func enrichUnmarshalError(err error) error {
+	var syntaxErr *json.SyntaxError
+	if errors.As(err, &syntaxErr) {
+		return fmt.Errorf("error at offset %d: %s", syntaxErr.Offset, syntaxErr.Error())
+	}
+	return err
+}
diff --git a/x/genutil/client/cli/validate_genesis_test.go b/x/genutil/client/cli/validate_genesis_test.go
index bd31a4b8ea..2608f448d5 100644
--- a/x/genutil/client/cli/validate_genesis_test.go
+++ b/x/genutil/client/cli/validate_genesis_test.go
@@ -6,9 +6,16 @@ import (
 
 	"github.com/stretchr/testify/require"
 
+	appmodulev2 "cosmossdk.io/core/appmodule/v2"
+	"cosmossdk.io/x/staking"
+
 	"github.com/cosmos/cosmos-sdk/client"
+	codectestutil "github.com/cosmos/cosmos-sdk/codec/testutil"
 	"github.com/cosmos/cosmos-sdk/testutil"
 	clitestutil "github.com/cosmos/cosmos-sdk/testutil/cli"
+	"github.com/cosmos/cosmos-sdk/types/module"
+	testutilmod "github.com/cosmos/cosmos-sdk/types/module/testutil"
+	"github.com/cosmos/cosmos-sdk/x/genutil"
 	"github.com/cosmos/cosmos-sdk/x/genutil/client/cli"
 )
 
@@ -32,15 +39,37 @@ var v037Exported = `{
 }`
 
 func TestValidateGenesis(t *testing.T) {
+	cdc := testutilmod.MakeTestEncodingConfig(codectestutil.CodecOptions{}, genutil.AppModule{}).Codec
 	testCases := []struct {
-		name    string
-		genesis string
-		expErr  bool
+		name      string
+		genesis   string
+		expErrStr string
+		genMM     *module.Manager
 	}{
+		{
+			"invalid json",
+			`{"app_state": {x,}}`,
+			"error at offset 16: invalid character",
+			module.NewManagerFromMap(nil),
+		},
+		{
+			"invalid: missing module config in app_state",
+			func() string {
+				bz, err := os.ReadFile("../../types/testdata/app_genesis.json")
+				require.NoError(t, err)
+
+				return string(bz)
+			}(),
+			"section is missing in the app_state",
+			module.NewManagerFromMap(map[string]appmodulev2.AppModule{
+				"custommod": staking.NewAppModule(cdc, nil, nil, nil),
+			}),
+		},
 		{
 			"exported 0.37 genesis file",
 			v037Exported,
-			true,
+			"make sure that you have correctly migrated all CometBFT consensus params",
+			module.NewManagerFromMap(nil),
 		},
 		{
 			"valid 0.50 genesis file",
@@ -50,7 +79,8 @@ func TestValidateGenesis(t *testing.T) {
 
 				return string(bz)
 			}(),
-			false,
+			"",
+			module.NewManagerFromMap(nil),
 		},
 	}
 
@@ -59,9 +89,9 @@ func TestValidateGenesis(t *testing.T) {
 
 		t.Run(tc.name, func(t *testing.T) {
 			genesisFile := testutil.WriteToNewTempFile(t, tc.genesis)
-			_, err := clitestutil.ExecTestCLICmd(client.Context{}, cli.ValidateGenesisCmd(nil), []string{genesisFile.Name()})
-			if tc.expErr {
-				require.Contains(t, err.Error(), "make sure that you have correctly migrated all CometBFT consensus params")
+			_, err := clitestutil.ExecTestCLICmd(client.Context{}, cli.ValidateGenesisCmd(tc.genMM), []string{genesisFile.Name()})
+			if tc.expErrStr != "" {
+				require.Contains(t, err.Error(), tc.expErrStr)
 			} else {
 				require.NoError(t, err)
 			}