diff --git a/.github/CODEOWNERS b/.github/CODEOWNERS
index b957029a8c5..a0f63e8c536 100644
--- a/.github/CODEOWNERS
+++ b/.github/CODEOWNERS
@@ -897,6 +897,7 @@
 /packages/wallet/src/initialization/instances/keyring-controller/                @MetaMask/accounts-engineers @MetaMask/core-platform
 /packages/wallet/src/initialization/instances/logging-controller/                @MetaMask/confirmations
 /packages/wallet/src/initialization/instances/network-controller/                @MetaMask/core-platform @MetaMask/metamask-assets
+/packages/wallet/src/initialization/instances/network-enablement-controller/     @MetaMask/metamask-assets
 /packages/wallet/src/initialization/instances/passkey-controller/                @MetaMask/web3auth
 /packages/wallet/src/initialization/instances/permission-controller/             @MetaMask/core-platform
 /packages/wallet/src/initialization/instances/remote-feature-flag-controller/    @MetaMask/core-platform @MetaMask/extension-platform @MetaMask/mobile-platform
diff --git a/codeowners.ts b/codeowners.ts
index 1e174a68620..e3e9a39af66 100644
--- a/codeowners.ts
+++ b/codeowners.ts
@@ -258,6 +258,7 @@ const config = {
     },
     'network-enablement-controller': {
       teams: ['@MetaMask/metamask-assets'],
+      initializationPath: 'network-enablement-controller',
     },
     'node-utils': {
       teams: ['@MetaMask/core-platform'],
diff --git a/packages/network-enablement-controller/CHANGELOG.md b/packages/network-enablement-controller/CHANGELOG.md
index ddda33e6cfd..b4bcb5140eb 100644
--- a/packages/network-enablement-controller/CHANGELOG.md
+++ b/packages/network-enablement-controller/CHANGELOG.md
@@ -22,6 +22,7 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ### Fixed
 
+- Import `@metamask/slip44` with a JSON import attribute so Node.js ESM consumers do not throw `ERR_IMPORT_ATTRIBUTE_MISSING` when importing `NetworkEnablementController` ([#10997](https://github.com/MetaMask/core/pull/10997))
 - Preserve existing network enablement when an auto-enabled network from the config registry is added ([#10763](https://github.com/MetaMask/core/pull/10763))
 
 ## [7.0.2]
diff --git a/packages/network-enablement-controller/src/services/Slip44Service.ts b/packages/network-enablement-controller/src/services/Slip44Service.ts
index affebea52c7..f83b10f1915 100644
--- a/packages/network-enablement-controller/src/services/Slip44Service.ts
+++ b/packages/network-enablement-controller/src/services/Slip44Service.ts
@@ -1,6 +1,9 @@
 import { fetchWithErrorHandling } from '@metamask/controller-utils';
+// `@metamask/slip44` publishes a JSON file as its entry point. Node.js ESM
+// rejects that import unless it carries a JSON import attribute, which crashes
+// the wallet daemon on Node 22 and 24.
 // @ts-expect-error: No type definitions for '@metamask/slip44'
-import slip44 from '@metamask/slip44';
+import slip44 from '@metamask/slip44' with { type: 'json' };
 
 const CHAINID_NETWORK_URL = 'https://chainid.network/chains.json';
 
diff --git a/packages/wallet/CHANGELOG.md b/packages/wallet/CHANGELOG.md
index d2efe17ef06..fab293d3b65 100644
--- a/packages/wallet/CHANGELOG.md
+++ b/packages/wallet/CHANGELOG.md
@@ -7,8 +7,15 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ## [Unreleased]
 
+### Added
+
+- **BREAKING:** Add `NetworkEnablementController` to the default initialization configurations ([#10997](https://github.com/MetaMask/core/pull/10997))
+  - Delegates `MultichainNetworkController:getState`. `Wallet` does not construct `MultichainNetworkController`. Clients must register that action on the wallet messenger before calling `wallet.init()`. `NetworkEnablementController.init()` reads it during `Wallet.init()`, and `enableAllPopularNetworks` and `listPopularMultichainNetworks` read it later.
+  - Also delegates `ConfigRegistryController:getState`, `NetworkController:getState`, `NetworkController:networkAdded`, `NetworkController:networkRemoved`, `NetworkController:stateChange`, and `TransactionController:transactionSubmitted`. `Wallet` constructs those controllers during default initialization.
+
 ### Changed
 
+- Add `@metamask/network-enablement-controller` as a dependency ([#10997](https://github.com/MetaMask/core/pull/10997))
 - Bump `@metamask/claims-controller` from `^1.0.4` to `^1.1.0` ([#11092](https://github.com/MetaMask/core/pull/11092))
 - Bump `@metamask/shield-controller` from `^7.0.5` to `^7.1.0` ([#11092](https://github.com/MetaMask/core/pull/11092))
 - Bump `@metamask/subscription-controller` from `^15.0.0` to `^15.1.0` ([#11092](https://github.com/MetaMask/core/pull/11092))
diff --git a/packages/wallet/package.json b/packages/wallet/package.json
index b4bcb42bbc2..655a98ed46f 100644
--- a/packages/wallet/package.json
+++ b/packages/wallet/package.json
@@ -67,6 +67,7 @@
     "@metamask/logging-controller": "^10.0.0",
     "@metamask/messenger": "^3.0.0",
     "@metamask/network-controller": "^37.1.1",
+    "@metamask/network-enablement-controller": "^7.0.2",
     "@metamask/passkey-controller": "^4.1.0",
     "@metamask/permission-controller": "^14.0.0",
     "@metamask/remote-feature-flag-controller": "^7.0.0",
diff --git a/packages/wallet/src/Wallet.test.ts b/packages/wallet/src/Wallet.test.ts
index 8714053046b..6a3033710f3 100644
--- a/packages/wallet/src/Wallet.test.ts
+++ b/packages/wallet/src/Wallet.test.ts
@@ -199,7 +199,7 @@ describe('Wallet', () => {
 
     const results = await wallet.init();
 
-    expect(results).toHaveLength(7);
+    expect(results).toHaveLength(8);
   });
 
   it('disallows modifying the messenger', async () => {
diff --git a/packages/wallet/src/initialization/instances/index.ts b/packages/wallet/src/initialization/instances/index.ts
index ea1694abb1d..4055cad6ada 100644
--- a/packages/wallet/src/initialization/instances/index.ts
+++ b/packages/wallet/src/initialization/instances/index.ts
@@ -14,6 +14,7 @@ export { geolocationController } from './geolocation-controller/geolocation-cont
 export { keyringController } from './keyring-controller/keyring-controller.js';
 export { loggingController } from './logging-controller/logging-controller.js';
 export { networkController } from './network-controller/network-controller.js';
+export { networkEnablementController } from './network-enablement-controller/network-enablement-controller.js';
 export { passkeyController } from './passkey-controller/passkey-controller.js';
 export { permissionController } from './permission-controller/permission-controller.js';
 export { subjectMetadataController } from './permission-controller/subject-metadata-controller.js';
diff --git a/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.test.ts b/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.test.ts
new file mode 100644
index 00000000000..eb14befe35a
--- /dev/null
+++ b/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.test.ts
@@ -0,0 +1,163 @@
+import { Messenger } from '@metamask/messenger';
+import { NetworkEnablementController } from '@metamask/network-enablement-controller';
+import type { NetworkEnablementControllerState } from '@metamask/network-enablement-controller';
+import { describe, expect, it, vi } from 'vitest';
+
+import { defaultConfigurations } from '../../defaults.js';
+import type {
+  DefaultActions,
+  DefaultEvents,
+  RootMessenger,
+} from '../../defaults.js';
+import { networkEnablementController } from './network-enablement-controller.js';
+
+type ActionHandler = (...args: unknown[]) => unknown;
+
+type AnyMessenger = Messenger<string>;
+
+const PERSISTED_STATE: NetworkEnablementControllerState = {
+  enabledNetworkMap: {
+    eip155: {
+      '0x1': false,
+    },
+  },
+  nativeAssetIdentifiers: {
+    'eip155:1': 'eip155:1/slip44:60',
+  },
+};
+
+/**
+ * Creates a root messenger for use in tests.
+ *
+ * @returns A root messenger.
+ */
+function getRootMessenger(): RootMessenger<DefaultActions, DefaultEvents> {
+  return new Messenger({ namespace: 'Root' });
+}
+
+describe('networkEnablementController', () => {
+  it('is registered as a default initialization configuration', () => {
+    expect(Object.values(defaultConfigurations)).toContain(
+      networkEnablementController,
+    );
+  });
+
+  it('initializes a NetworkEnablementController with default state', () => {
+    const messenger =
+      networkEnablementController.getMessenger(getRootMessenger());
+
+    const instance = networkEnablementController.init({
+      state: undefined,
+      messenger,
+      options: {},
+    });
+
+    expect(instance).toBeInstanceOf(NetworkEnablementController);
+    expect(instance.state.enabledNetworkMap.eip155?.['0x1']).toBe(true);
+    expect(instance.state.nativeAssetIdentifiers).toStrictEqual({});
+  });
+
+  it('forwards provided state over the defaults', () => {
+    const messenger =
+      networkEnablementController.getMessenger(getRootMessenger());
+
+    const instance = networkEnablementController.init({
+      state: PERSISTED_STATE,
+      messenger,
+      options: {},
+    });
+
+    expect(instance.state.enabledNetworkMap.eip155?.['0x1']).toBe(false);
+    expect(instance.state.nativeAssetIdentifiers).toStrictEqual(
+      PERSISTED_STATE.nativeAssetIdentifiers,
+    );
+  });
+
+  it('exposes its state through the root messenger', () => {
+    const rootMessenger = getRootMessenger();
+    const messenger = networkEnablementController.getMessenger(rootMessenger);
+
+    networkEnablementController.init({
+      state: undefined,
+      messenger,
+      options: {},
+    });
+
+    expect(
+      rootMessenger.call('NetworkEnablementController:getState')
+        .enabledNetworkMap.eip155?.['0x1'],
+    ).toBe(true);
+  });
+
+  it.each([
+    'ConfigRegistryController:getState',
+    'MultichainNetworkController:getState',
+    'NetworkController:getState',
+  ])('delegates the %s action', (actionType) => {
+    const rootMessenger = getRootMessenger();
+    const handler = vi.fn().mockReturnValue('result');
+    registerActionHandler(rootMessenger, actionType, handler);
+    const messenger = networkEnablementController.getMessenger(rootMessenger);
+
+    const result = (
+      messenger as unknown as { call(type: string): unknown }
+    ).call(actionType);
+
+    expect(handler).toHaveBeenCalledTimes(1);
+    expect(result).toBe('result');
+  });
+
+  it.each([
+    'NetworkController:networkAdded',
+    'NetworkController:networkRemoved',
+    'NetworkController:stateChange',
+    'TransactionController:transactionSubmitted',
+  ])('delegates the %s event', (eventType) => {
+    const rootMessenger = getRootMessenger();
+    const messenger = networkEnablementController.getMessenger(rootMessenger);
+    const listener = vi.fn();
+    (
+      messenger as unknown as {
+        subscribe(type: string, handler: ActionHandler): void;
+      }
+    ).subscribe(eventType, listener);
+
+    publishEvent(rootMessenger, eventType, 'payload');
+
+    expect(listener).toHaveBeenCalledWith('payload');
+  });
+});
+
+function registerActionHandler(
+  parent: RootMessenger<DefaultActions, DefaultEvents>,
+  actionType: string,
+  handler: ActionHandler,
+): void {
+  const messenger = new Messenger({
+    namespace: actionType.split(':')[0],
+    parent: parent as unknown as AnyMessenger,
+  });
+
+  (
+    messenger as unknown as {
+      registerActionHandler(type: string, handler: ActionHandler): void;
+    }
+  ).registerActionHandler(actionType, handler);
+}
+
+function publishEvent(
+  parent: RootMessenger<DefaultActions, DefaultEvents>,
+  eventType: string,
+  ...payload: unknown[]
+): void {
+  const messenger = new Messenger({
+    namespace: eventType.split(':')[0],
+    parent: parent as unknown as AnyMessenger,
+  });
+
+  (
+    messenger as unknown as {
+      publish(type: string, ...payload: unknown[]): void;
+    }
+  ).publish(eventType, ...payload);
+}
diff --git a/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.ts b/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.ts
new file mode 100644
index 00000000000..cef810b1e55
--- /dev/null
+++ b/packages/wallet/src/initialization/instances/network-enablement-controller/network-enablement-controller.ts
@@ -0,0 +1,41 @@
+import { Messenger } from '@metamask/messenger';
+import { NetworkEnablementController } from '@metamask/network-enablement-controller';
+import type { NetworkEnablementControllerMessenger } from '@metamask/network-enablement-controller';
+
+import type { InitializationConfiguration } from '../../types.js';
+
+export const networkEnablementController: InitializationConfiguration<
+  NetworkEnablementController,
+  NetworkEnablementControllerMessenger
+> = {
+  name: 'NetworkEnablementController',
+  reference: NetworkEnablementController,
+  init: ({ state, messenger }) =>
+    new NetworkEnablementController({
+      state,
+      messenger,
+    }),
+  getMessenger: (parent) => {
+    const messenger: NetworkEnablementControllerMessenger = new Messenger({
+      namespace: 'NetworkEnablementController',
+      parent,
+    });
+
+    parent.delegate({
+      messenger,
+      actions: [
+        'ConfigRegistryController:getState',
+        'MultichainNetworkController:getState',
+        'NetworkController:getState',
+      ],
+      events: [
+        'NetworkController:networkAdded',
+        'NetworkController:networkRemoved',
+        'NetworkController:stateChange',
+        'TransactionController:transactionSubmitted',
+      ],
+    });
+
+    return messenger;
+  },
+};
diff --git a/packages/wallet/tsconfig.build.json b/packages/wallet/tsconfig.build.json
index 00bdbbf398d..dfdc85cf60f 100644
--- a/packages/wallet/tsconfig.build.json
+++ b/packages/wallet/tsconfig.build.json
@@ -50,6 +50,9 @@
     {
       "path": "../network-controller/tsconfig.build.json"
     },
+    {
+      "path": "../network-enablement-controller/tsconfig.build.json"
+    },
     {
       "path": "../passkey-controller/tsconfig.build.json"
     },
diff --git a/packages/wallet/tsconfig.json b/packages/wallet/tsconfig.json
index 70f5feb27be..d16557d7cd7 100644
--- a/packages/wallet/tsconfig.json
+++ b/packages/wallet/tsconfig.json
@@ -46,6 +46,9 @@
     {
       "path": "../network-controller"
     },
+    {
+      "path": "../network-enablement-controller"
+    },
     {
       "path": "../passkey-controller"
     },
diff --git a/packages/wallet/tsconfig.lint.json b/packages/wallet/tsconfig.lint.json
index 3d3d9d2b590..ae0727ede27 100644
--- a/packages/wallet/tsconfig.lint.json
+++ b/packages/wallet/tsconfig.lint.json
@@ -53,6 +53,9 @@
     {
       "path": "../network-controller/tsconfig.lint.json"
     },
+    {
+      "path": "../network-enablement-controller/tsconfig.lint.json"
+    },
     {
       "path": "../passkey-controller/tsconfig.lint.json"
     },
diff --git a/yarn.lock b/yarn.lock
index 48a291b9e37..921ad40bbfa 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -9163,6 +9163,7 @@ __metadata:
     "@metamask/logging-controller": "npm:^10.0.0"
     "@metamask/messenger": "npm:^3.0.0"
     "@metamask/network-controller": "npm:^37.1.1"
+    "@metamask/network-enablement-controller": "npm:^7.0.2"
     "@metamask/passkey-controller": "npm:^4.1.0"
     "@metamask/permission-controller": "npm:^14.0.0"
     "@metamask/remote-feature-flag-controller": "npm:^7.0.0"