diff --git a/packages/network-controller/CHANGELOG.md b/packages/network-controller/CHANGELOG.md
index 77dc401045b..2f5a8890843 100644
--- a/packages/network-controller/CHANGELOG.md
+++ b/packages/network-controller/CHANGELOG.md
@@ -37,6 +37,10 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
   - Bump `@metamask/eth-json-rpc-infura` to `^10.1.0`
   - Bump `@metamask/eth-json-rpc-middleware` to `^15.1.0`
 
+### Fixed
+
+- Fix `findNetworkClientIdByChainId` to return the network client ID for the chain's configured default RPC endpoint instead of its first listed RPC endpoint ([#5344](https://github.com/MetaMask/core/pull/5344))
+
 ## [22.2.1]
 
 ### Changed
diff --git a/packages/network-controller/src/NetworkController.ts b/packages/network-controller/src/NetworkController.ts
index 73ac9d96631..4a6e38c0867 100644
--- a/packages/network-controller/src/NetworkController.ts
+++ b/packages/network-controller/src/NetworkController.ts
@@ -2100,20 +2100,27 @@ export class NetworkController extends BaseController<
   }
 
   /**
-   * Searches for a network configuration ID with the given ChainID and returns it.
+   * Searches for the default RPC endpoint configured for the given chain and
+   * returns its network client ID. This can then be passed to
+   * {@link getNetworkClientById} to retrieve the network client.
    *
-   * @param chainId - ChainId to search for
-   * @returns networkClientId of the network configuration with the given chainId
+   * @param chainId - Chain ID to search for.
+   * @returns The ID of the network client created for the chain's default RPC
+   * endpoint.
    */
   findNetworkClientIdByChainId(chainId: Hex): NetworkClientId {
-    const networkClients = this.getNetworkClientRegistry();
-    const networkClientEntry = Object.entries(networkClients).find(
-      ([_, networkClient]) => networkClient.configuration.chainId === chainId,
-    );
-    if (networkClientEntry === undefined) {
-      throw new Error("Couldn't find networkClientId for chainId");
+    const networkConfiguration =
+      this.state.networkConfigurationsByChainId[chainId];
+
+    if (!networkConfiguration) {
+      throw new Error(`Invalid chain ID "${chainId}"`);
     }
-    return networkClientEntry[0];
+
+    const { networkClientId } =
+      networkConfiguration.rpcEndpoints[
+        networkConfiguration.defaultRpcEndpointIndex
+      ];
+    return networkClientId;
   }
 
   /**
diff --git a/packages/network-controller/tests/NetworkController.test.ts b/packages/network-controller/tests/NetworkController.test.ts
index e11448fc2d9..4b65a01f642 100644
--- a/packages/network-controller/tests/NetworkController.test.ts
+++ b/packages/network-controller/tests/NetworkController.test.ts
@@ -969,48 +969,81 @@ describe('NetworkController', () => {
     });
   });
 
-  describe('findNetworkConfigurationByChainId', () => {
-    it('returns the network configuration for the given chainId', async () => {
+  describe.each([
+    [
+      'findNetworkClientIdByChainId',
+      (
+        {
+          controller,
+        }: {
+          controller: NetworkController;
+        },
+        args: Parameters<NetworkController['findNetworkClientIdByChainId']>,
+      ): ReturnType<NetworkController['findNetworkClientIdByChainId']> =>
+        controller.findNetworkClientIdByChainId(...args),
+    ],
+    [
+      'NetworkController:findNetworkClientIdByChainId',
+      (
+        {
+          messenger,
+        }: {
+          messenger: Messenger<
+            NetworkControllerActions,
+            NetworkControllerEvents
+          >;
+        },
+        args: Parameters<NetworkController['findNetworkClientIdByChainId']>,
+      ): ReturnType<NetworkController['findNetworkClientIdByChainId']> =>
+        messenger.call(
+          'NetworkController:findNetworkClientIdByChainId',
+          ...args,
+        ),
+    ],
+  ])('%s', (_desc, findNetworkClientIdByChainId) => {
+    it('returns the ID of the network client corresponding to the default RPC endpoint for the given chain', async () => {
       await withController(
-        { infuraProjectId: 'some-infura-project-id' },
-        async ({ controller }) => {
-          const fakeNetworkClient = buildFakeClient();
-          mockCreateNetworkClient().mockReturnValue(fakeNetworkClient);
-
-          const networkClientId =
-            controller.findNetworkClientIdByChainId('0x1');
-          expect(networkClientId).toBe('mainnet');
+        {
+          state: buildNetworkControllerStateWithDefaultSelectedNetworkClientId({
+            networkConfigurationsByChainId: {
+              '0x1337': buildCustomNetworkConfiguration({
+                chainId: '0x1337' as const,
+                defaultRpcEndpointIndex: 1,
+                rpcEndpoints: [
+                  {
+                    name: 'Test Endpoint 1',
+                    networkClientId: 'AAAA-AAAA-AAAA-AAAA',
+                    url: 'https://test.network/1',
+                    type: RpcEndpointType.Custom,
+                  },
+                  {
+                    name: 'Test Endpoint 2',
+                    networkClientId: 'BBBB-BBBB-BBBB-BBBB',
+                    url: 'https://test.network/2',
+                    type: RpcEndpointType.Custom,
+                  },
+                ],
+              }),
+            },
+          }),
         },
-      );
-    });
+        ({ controller, messenger }) => {
+          const networkClientId = findNetworkClientIdByChainId(
+            { controller, messenger },
+            ['0x1337'],
+          );
 
-    it('throws if the chainId doesnt exist in the configuration', async () => {
-      await withController(
-        { infuraProjectId: 'some-infura-project-id' },
-        async ({ controller }) => {
-          const fakeNetworkClient = buildFakeClient();
-          mockCreateNetworkClient().mockReturnValue(fakeNetworkClient);
-          expect(() =>
-            controller.findNetworkClientIdByChainId('0xdeadbeef'),
-          ).toThrow("Couldn't find networkClientId for chainId");
+          expect(networkClientId).toBe('BBBB-BBBB-BBBB-BBBB');
         },
       );
     });
 
-    it('is callable from the controller messenger', async () => {
-      await withController(
-        { infuraProjectId: 'some-infura-project-id' },
-        async ({ messenger }) => {
-          const fakeNetworkClient = buildFakeClient();
-          mockCreateNetworkClient().mockReturnValue(fakeNetworkClient);
-
-          const networkClientId = messenger.call(
-            'NetworkController:findNetworkClientIdByChainId',
-            '0x1',
-          );
-          expect(networkClientId).toBe('mainnet');
-        },
-      );
+    it('throws if there are no network clients registered for the given chain', async () => {
+      await withController(({ controller, messenger }) => {
+        expect(() =>
+          findNetworkClientIdByChainId({ controller, messenger }, ['0x999999']),
+        ).toThrow('Invalid chain ID "0x999999"');
+      });
     });
   });