diff --git a/packages/chain-agnostic-permission/CHANGELOG.md b/packages/chain-agnostic-permission/CHANGELOG.md
index f025aa5a44a..ee3a3ba4bb7 100644
--- a/packages/chain-agnostic-permission/CHANGELOG.md
+++ b/packages/chain-agnostic-permission/CHANGELOG.md
@@ -11,6 +11,7 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 - Bump `@metamask/network-controller` to `^23.4.0` ([#5765](https://github.com/MetaMask/core/pull/5765))
 - Bump `@metamask/controller-utils` to `^11.8.0` ([#5765](https://github.com/MetaMask/core/pull/5765))
+- Change `caip25CaveatBuilder` to list unsupported scopes in the unsupported scopes error ([#5806](https://github.com/MetaMask/core/pull/5806))
 
 ## [0.6.0]
 
diff --git a/packages/chain-agnostic-permission/src/caip25Permission.test.ts b/packages/chain-agnostic-permission/src/caip25Permission.test.ts
index d7627ed4606..9823811eb15 100644
--- a/packages/chain-agnostic-permission/src/caip25Permission.test.ts
+++ b/packages/chain-agnostic-permission/src/caip25Permission.test.ts
@@ -744,7 +744,7 @@ describe('caip25CaveatBuilder', () => {
       });
     }).toThrow(
       new Error(
-        `${Caip25EndowmentPermissionName} error: Received scopeString value(s) for caveat of type "${Caip25CaveatType}" that are not supported by the wallet.`,
+        `${Caip25EndowmentPermissionName} error: Received scopeString value(s): eip155:1, bip122:000000000019d6689c085ae165831e93, eip155:5, bip122:12a765e31ffd4059bada1e25190f6e98 for caveat of type "${Caip25CaveatType}" that are not supported by the wallet.`,
       ),
     );
   });
diff --git a/packages/chain-agnostic-permission/src/caip25Permission.ts b/packages/chain-agnostic-permission/src/caip25Permission.ts
index 3d709418901..44a90150a72 100644
--- a/packages/chain-agnostic-permission/src/caip25Permission.ts
+++ b/packages/chain-agnostic-permission/src/caip25Permission.ts
@@ -220,23 +220,20 @@ export const caip25CaveatBuilder = ({
         }
       };
 
-      const allRequiredScopesSupported = Object.keys(requiredScopes).every(
+      const unsupportedScopes = Object.keys({
+        ...requiredScopes,
+        ...optionalScopes,
+      }).filter(
         (scopeString) =>
-          isSupportedScopeString(scopeString, {
+          !isSupportedScopeString(scopeString, {
             isEvmChainIdSupported,
             isNonEvmScopeSupported,
           }),
       );
-      const allOptionalScopesSupported = Object.keys(optionalScopes).every(
-        (scopeString) =>
-          isSupportedScopeString(scopeString, {
-            isEvmChainIdSupported,
-            isNonEvmScopeSupported,
-          }),
-      );
-      if (!allRequiredScopesSupported || !allOptionalScopesSupported) {
+
+      if (unsupportedScopes.length > 0) {
         throw new Error(
-          `${Caip25EndowmentPermissionName} error: Received scopeString value(s) for caveat of type "${Caip25CaveatType}" that are not supported by the wallet.`,
+          `${Caip25EndowmentPermissionName} error: Received scopeString value(s): ${unsupportedScopes.join(', ')} for caveat of type "${Caip25CaveatType}" that are not supported by the wallet.`,
         );
       }