diff --git a/README.md b/README.md
index 54235840db..dff073e7f2 100644
--- a/README.md
+++ b/README.md
@@ -424,6 +424,7 @@ linkStyle default opacity:0.5
   network_controller --> eth_json_rpc_provider;
   network_controller --> json_rpc_engine;
   network_controller --> messenger;
+  network_controller --> remote_feature_flag_controller;
   network_enablement_controller --> base_controller;
   network_enablement_controller --> controller_utils;
   network_enablement_controller --> messenger;
diff --git a/packages/network-controller/CHANGELOG.md b/packages/network-controller/CHANGELOG.md
index 14e4113c13..6c4b4eee3a 100644
--- a/packages/network-controller/CHANGELOG.md
+++ b/packages/network-controller/CHANGELOG.md
@@ -17,6 +17,13 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
   - The default `pollingInterval` for the block tracker is now `20` seconds.
   - The default `retryTimeout` for the block tracker is now `20` seconds.
 
+### Changed
+
+- **BREAKING:** Automatically populate `isRpcFailoverEnabled` using `RemoteFeatureFlagController` ([#9013](https://github.com/MetaMask/core/pull/9013))
+  - `NetworkController.init` must now be called to fully initialize the controller.
+  - The constructor argument `isRpcFailoverEnabled` is no longer available.
+  - `RemoteFeatureFlagController:stateChange` and `RemoteFeatureFlagController:getState` are now required.
+
 ### Fixed
 
 - Add defaults for `fetch`, `btoa` and `isOffline` in `RpcServiceOptions` ([#9000](https://github.com/MetaMask/core/pull/9000))
diff --git a/packages/network-controller/package.json b/packages/network-controller/package.json
index d48d99f683..9089ebb71e 100644
--- a/packages/network-controller/package.json
+++ b/packages/network-controller/package.json
@@ -63,6 +63,7 @@
     "@metamask/eth-query": "^4.0.0",
     "@metamask/json-rpc-engine": "^10.5.0",
     "@metamask/messenger": "^1.2.0",
+    "@metamask/remote-feature-flag-controller": "^4.2.2",
     "@metamask/rpc-errors": "^7.0.2",
     "@metamask/swappable-obj-proxy": "^2.3.0",
     "@metamask/utils": "^11.9.0",
diff --git a/packages/network-controller/src/NetworkController.ts b/packages/network-controller/src/NetworkController.ts
index 4cc4397e7a..2cc779140f 100644
--- a/packages/network-controller/src/NetworkController.ts
+++ b/packages/network-controller/src/NetworkController.ts
@@ -21,6 +21,10 @@ import {
 import type { PollingBlockTrackerOptions } from '@metamask/eth-block-tracker';
 import EthQuery from '@metamask/eth-query';
 import type { Messenger } from '@metamask/messenger';
+import {
+  RemoteFeatureFlagControllerGetStateAction,
+  RemoteFeatureFlagControllerStateChangeEvent,
+} from '@metamask/remote-feature-flag-controller';
 import { errorCodes } from '@metamask/rpc-errors';
 import {
   createEventEmitterProxy,
@@ -55,6 +59,7 @@ import type {
   NetworkControllerMethodActions,
 } from './NetworkController-method-action-types';
 import type { RpcServiceOptionsWithDefaults } from './rpc-service/rpc-service';
+import { getIsRpcFailoverEnabled } from './selectors';
 import { NetworkClientType } from './types';
 import type {
   BlockTracker,
@@ -663,7 +668,7 @@ export type NetworkControllerEvents =
 /**
  * All events that {@link NetworkController} calls internally.
  */
-type AllowedEvents = never;
+type AllowedEvents = RemoteFeatureFlagControllerStateChangeEvent;
 
 const MESSENGER_EXPOSED_METHODS = [
   'addNetwork',
@@ -714,7 +719,9 @@ export type NetworkControllerGetNetworkConfigurationByNetworkClientId =
 /**
  * All actions that {@link NetworkController} calls internally.
  */
-type AllowedActions = ConnectivityControllerGetStateAction;
+type AllowedActions =
+  | ConnectivityControllerGetStateAction
+  | RemoteFeatureFlagControllerGetStateAction;
 
 export type NetworkControllerMessenger = Messenger<
   typeof controllerName,
@@ -767,11 +774,6 @@ export type NetworkControllerOptions = {
    * An array of Hex Chain IDs representing the additional networks to be included as default.
    */
   additionalDefaultNetworks?: AdditionalDefaultNetwork[];
-  /**
-   * Whether or not requests sent to unavailable RPC endpoints should be
-   * automatically diverted to configured failover RPC endpoints.
-   */
-  isRpcFailoverEnabled?: boolean;
 };
 
 /**
@@ -1295,10 +1297,7 @@ export class NetworkController extends BaseController<
     NetworkConfiguration
   >;
 
-  #isRpcFailoverEnabled: Exclude<
-    NetworkControllerOptions['isRpcFailoverEnabled'],
-    undefined
-  >;
+  #isRpcFailoverEnabled = false;
 
   /**
    * Constructs a NetworkController.
@@ -1314,7 +1313,6 @@ export class NetworkController extends BaseController<
       getRpcServiceOptions,
       getBlockTrackerOptions,
       additionalDefaultNetworks,
-      isRpcFailoverEnabled = false,
     } = options;
     const initialState = {
       ...getDefaultNetworkControllerState(additionalDefaultNetworks),
@@ -1357,7 +1355,6 @@ export class NetworkController extends BaseController<
     this.#log = log;
     this.#getRpcServiceOptions = getRpcServiceOptions;
     this.#getBlockTrackerOptions = getBlockTrackerOptions;
-    this.#isRpcFailoverEnabled = isRpcFailoverEnabled;
 
     this.#previouslySelectedNetworkClientId =
       this.state.selectedNetworkClientId;
@@ -1395,6 +1392,15 @@ export class NetworkController extends BaseController<
         });
       },
     );
+
+    this.messenger.subscribe(
+      // eslint-disable-next-line no-restricted-syntax
+      'RemoteFeatureFlagController:stateChange',
+      (isRpcFailoverEnabled) => {
+        this.#updateRpcFailoverEnabled(isRpcFailoverEnabled);
+      },
+      getIsRpcFailoverEnabled,
+    );
   }
 
   /**
@@ -1626,6 +1632,14 @@ export class NetworkController extends BaseController<
     await this.lookupNetwork();
   }
 
+  /**
+   * Initialize the NetworkController, updating the RPC failover feature flag.
+   */
+  init(): void {
+    const state = this.messenger.call('RemoteFeatureFlagController:getState');
+    this.#updateRpcFailoverEnabled(getIsRpcFailoverEnabled(state));
+  }
+
   /**
    * Creates proxies for accessing the global network client and its block
    * tracker. You must call this method in order to use
diff --git a/packages/network-controller/src/selectors.ts b/packages/network-controller/src/selectors.ts
new file mode 100644
index 0000000000..016c8a66b0
--- /dev/null
+++ b/packages/network-controller/src/selectors.ts
@@ -0,0 +1,9 @@
+import { RemoteFeatureFlagControllerState } from '@metamask/remote-feature-flag-controller';
+
+export function getIsRpcFailoverEnabled(
+  state: RemoteFeatureFlagControllerState,
+): boolean {
+  const walletFrameworkRpcFailoverEnabled = state.remoteFeatureFlags
+    .walletFrameworkRpcFailoverEnabled as boolean | undefined;
+  return walletFrameworkRpcFailoverEnabled ?? false;
+}
diff --git a/packages/network-controller/tests/NetworkController.test.ts b/packages/network-controller/tests/NetworkController.test.ts
index 487f87d4b2..cb36cd2edc 100644
--- a/packages/network-controller/tests/NetworkController.test.ts
+++ b/packages/network-controller/tests/NetworkController.test.ts
@@ -1131,6 +1131,23 @@ describe('NetworkController', () => {
   describe('disableRpcFailover', () => {
     describe('if the controller was initialized with isRpcFailoverEnabled = true', () => {
       it('calls disableRpcFailover on only the network clients whose RPC endpoints have configured failover URLs', async () => {
+        const originalCreateAutoManagedNetworkClient =
+          createAutoManagedNetworkClientModule.createAutoManagedNetworkClient;
+        const autoManagedNetworkClients: AutoManagedNetworkClient<NetworkClientConfiguration>[] =
+          [];
+        jest
+          .spyOn(
+            createAutoManagedNetworkClientModule,
+            'createAutoManagedNetworkClient',
+          )
+          .mockImplementation((...args) => {
+            const autoManagedNetworkClient =
+              originalCreateAutoManagedNetworkClient(...args);
+            jest.spyOn(autoManagedNetworkClient, 'disableRpcFailover');
+            autoManagedNetworkClients.push(autoManagedNetworkClient);
+            return autoManagedNetworkClient;
+          });
+
         await withController(
           {
             isRpcFailoverEnabled: true,
@@ -1171,23 +1188,6 @@ describe('NetworkController', () => {
             },
           },
           async ({ controller }) => {
-            const originalCreateAutoManagedNetworkClient =
-              createAutoManagedNetworkClientModule.createAutoManagedNetworkClient;
-            const autoManagedNetworkClients: AutoManagedNetworkClient<NetworkClientConfiguration>[] =
-              [];
-            jest
-              .spyOn(
-                createAutoManagedNetworkClientModule,
-                'createAutoManagedNetworkClient',
-              )
-              .mockImplementation((...args) => {
-                const autoManagedNetworkClient =
-                  originalCreateAutoManagedNetworkClient(...args);
-                jest.spyOn(autoManagedNetworkClient, 'disableRpcFailover');
-                autoManagedNetworkClients.push(autoManagedNetworkClient);
-                return autoManagedNetworkClient;
-              });
-
             controller.disableRpcFailover();
 
             expect(autoManagedNetworkClients).toHaveLength(3);
diff --git a/packages/network-controller/tests/helpers.ts b/packages/network-controller/tests/helpers.ts
index 860eb2a534..fb9f80cda5 100644
--- a/packages/network-controller/tests/helpers.ts
+++ b/packages/network-controller/tests/helpers.ts
@@ -89,12 +89,15 @@ export const TESTNET = {
  * @param options - Optional configuration.
  * @param options.connectivityStatus - The connectivity status to return by default.
  * If not provided, defaults to Online.
+ * @param options.isRpcFailoverEnabled - The RPC failover feature flag to return, defaults to false.
  * @returns The messenger.
  */
 export function buildRootMessenger({
   connectivityStatus = CONNECTIVITY_STATUSES.Online,
+  isRpcFailoverEnabled = false,
 }: {
   connectivityStatus?: ConnectivityStatus;
+  isRpcFailoverEnabled?: boolean;
 } = {}): RootMessenger {
   const rootMessenger = new Messenger<
     MockAnyNamespace,
@@ -109,6 +112,16 @@ export function buildRootMessenger({
     }),
   );
 
+  rootMessenger.registerActionHandler(
+    'RemoteFeatureFlagController:getState',
+    () => ({
+      remoteFeatureFlags: {
+        walletFrameworkRpcFailoverEnabled: isRpcFailoverEnabled,
+      },
+      cacheTimestamp: 0,
+    }),
+  );
+
   return rootMessenger;
 }
 
@@ -133,7 +146,12 @@ export function buildNetworkControllerMessenger(
 
   rootMessenger.delegate({
     messenger: networkControllerMessenger,
-    actions: ['ConnectivityController:getState'],
+    actions: [
+      'ConnectivityController:getState',
+      'RemoteFeatureFlagController:getState',
+    ],
+    // eslint-disable-next-line no-restricted-syntax
+    events: ['RemoteFeatureFlagController:stateChange'],
   });
 
   return networkControllerMessenger;
@@ -612,7 +630,9 @@ type WithControllerCallback<ReturnValue> = ({
   networkControllerMessenger: NetworkControllerMessenger;
 }) => Promise<ReturnValue> | ReturnValue;
 
-type WithControllerOptions = Partial<NetworkControllerOptions>;
+type WithControllerOptions = Partial<NetworkControllerOptions> & {
+  isRpcFailoverEnabled?: boolean;
+};
 
 type WithControllerArgs<ReturnValue> =
   | [WithControllerCallback<ReturnValue>]
@@ -632,7 +652,8 @@ export async function withController<ReturnValue>(
   ...args: WithControllerArgs<ReturnValue>
 ): Promise<ReturnValue> {
   const [{ ...rest }, fn] = args.length === 2 ? args : [{}, args[0]];
-  const messenger = buildRootMessenger();
+  const { isRpcFailoverEnabled, ...controllerOptions } = rest;
+  const messenger = buildRootMessenger({ isRpcFailoverEnabled });
   const networkControllerMessenger = buildNetworkControllerMessenger(messenger);
   const controller = new NetworkController({
     messenger: networkControllerMessenger,
@@ -645,8 +666,11 @@ export async function withController<ReturnValue>(
       btoa,
       isOffline: (): boolean => false,
     }),
-    ...rest,
+    ...controllerOptions,
   });
+
+  controller.init();
+
   try {
     return await fn({ controller, messenger, networkControllerMessenger });
   } finally {
diff --git a/packages/network-controller/tsconfig.build.json b/packages/network-controller/tsconfig.build.json
index 0ebc69f899..5767f283bb 100644
--- a/packages/network-controller/tsconfig.build.json
+++ b/packages/network-controller/tsconfig.build.json
@@ -13,7 +13,8 @@
     { "path": "../eth-json-rpc-middleware/tsconfig.build.json" },
     { "path": "../eth-json-rpc-provider/tsconfig.build.json" },
     { "path": "../json-rpc-engine/tsconfig.build.json" },
-    { "path": "../messenger/tsconfig.build.json" }
+    { "path": "../messenger/tsconfig.build.json" },
+    { "path": "../remote-feature-flag-controller/tsconfig.build.json" }
   ],
   "include": ["../../types", "./src"]
 }
diff --git a/packages/network-controller/tsconfig.json b/packages/network-controller/tsconfig.json
index 37d8a33ef5..87d6f24f68 100644
--- a/packages/network-controller/tsconfig.json
+++ b/packages/network-controller/tsconfig.json
@@ -12,7 +12,8 @@
     { "path": "../eth-json-rpc-middleware" },
     { "path": "../eth-json-rpc-provider" },
     { "path": "../json-rpc-engine" },
-    { "path": "../messenger" }
+    { "path": "../messenger" },
+    { "path": "../remote-feature-flag-controller" }
   ],
   "include": ["../../types", "../../tests", "./src", "./tests"]
 }
diff --git a/yarn.lock b/yarn.lock
index 4d08c1d875..d4405d370f 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -7658,6 +7658,7 @@ __metadata:
     "@metamask/eth-query": "npm:^4.0.0"
     "@metamask/json-rpc-engine": "npm:^10.5.0"
     "@metamask/messenger": "npm:^1.2.0"
+    "@metamask/remote-feature-flag-controller": "npm:^4.2.2"
     "@metamask/rpc-errors": "npm:^7.0.2"
     "@metamask/swappable-obj-proxy": "npm:^2.3.0"
     "@metamask/utils": "npm:^11.9.0"