diff --git a/packages/snaps-controllers/src/snaps/SnapController.test.tsx b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
index a23085242b..ddabf00d96 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.test.tsx
+++ b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
@@ -10624,6 +10624,8 @@ describe('SnapController', () => {
 
       await waitForStateChange(messenger);
 
+      await waitForStateChange(messenger);
+
       expect(snapController.isRunning(MOCK_SNAP_ID)).toBe(true);
 
       await new Promise((resolve) => setTimeout(resolve, 100));
@@ -10647,6 +10649,7 @@ describe('SnapController', () => {
       );
 
       expect(snapController.state).toStrictEqual({
+        isReady: false,
         snaps: {},
         snapStates: {},
         unencryptedSnapStates: {},
@@ -10769,6 +10772,23 @@ describe('SnapController', () => {
 
   describe('SnapController actions', () => {
     describe('SnapController:init', () => {
+      it('populates `isReady`', async () => {
+        const rootMessenger = getControllerMessenger();
+        const messenger = getSnapControllerMessenger(rootMessenger);
+
+        const snapController = getSnapController(
+          getSnapControllerOptions({ messenger }),
+        );
+
+        expect(snapController.state.isReady).toBe(false);
+        messenger.call('SnapController:init');
+
+        await waitForStateChange(messenger);
+        expect(snapController.state.isReady).toBe(true);
+
+        snapController.destroy();
+      });
+
       it('calls `onStart` for all Snaps with the `endowment:lifecycle-hooks` permission', async () => {
         const rootMessenger = getControllerMessenger();
         const messenger = getSnapControllerMessenger(rootMessenger);
@@ -12997,7 +13017,11 @@ describe('SnapController', () => {
           controller.metadata,
           'includeInDebugSnapshot',
         ),
-      ).toMatchInlineSnapshot(`{}`);
+      ).toMatchInlineSnapshot(`
+        {
+          "isReady": false,
+        }
+      `);
     });
 
     describe('includeInStateLogs', () => {
@@ -13012,6 +13036,7 @@ describe('SnapController', () => {
           ),
         ).toMatchInlineSnapshot(`
           {
+            "isReady": false,
             "snaps": {},
           }
         `);
diff --git a/packages/snaps-controllers/src/snaps/SnapController.ts b/packages/snaps-controllers/src/snaps/SnapController.ts
index 7b32f7a754..eb16034a41 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.ts
+++ b/packages/snaps-controllers/src/snaps/SnapController.ts
@@ -318,6 +318,7 @@ export type SnapControllerState = {
   snaps: StoredSnaps;
   snapStates: Record<SnapId, string | null>;
   unencryptedSnapStates: Record<SnapId, string | null>;
+  isReady: boolean;
 };
 
 export type PersistedSnapControllerState = SnapControllerState & {
@@ -854,6 +855,7 @@ const defaultState: SnapControllerState = {
   snaps: {},
   snapStates: {},
   unencryptedSnapStates: {},
+  isReady: false,
 };
 
 /**
@@ -965,6 +967,12 @@ export class SnapController extends BaseController<
     super({
       messenger,
       metadata: {
+        isReady: {
+          includeInStateLogs: true,
+          includeInDebugSnapshot: true,
+          persist: false,
+          usedInUi: false,
+        },
         snapStates: {
           includeInStateLogs: false,
           persist: true,
@@ -1327,6 +1335,9 @@ export class SnapController extends BaseController<
    * runnable Snaps.
    */
   init() {
+    // Lazily populate the `isReady` state.
+    this.#ensureCanUsePlatform().catch(logWarning);
+
     this.#callLifecycleHooks(METAMASK_ORIGIN, HandlerType.OnStart);
   }
 
@@ -1537,7 +1548,7 @@ export class SnapController extends BaseController<
    * Also updates any preinstalled Snaps to the latest allowlisted version.
    */
   async updateRegistry(): Promise<void> {
-    await this.#assertCanUsePlatform();
+    await this.#ensureCanUsePlatform();
     await this.messenger.call('SnapsRegistry:update');
 
     const blockedSnaps = await this.messenger.call(
@@ -1717,13 +1728,23 @@ export class SnapController extends BaseController<
   /**
    * Waits for onboarding and then asserts whether the Snaps platform is allowed to run.
    */
-  async #assertCanUsePlatform() {
+  async #ensureCanUsePlatform() {
     // Ensure the user has onboarded before allowing access to Snaps.
     await this.#ensureOnboardingComplete();
 
     const flags = this.#getFeatureFlags();
+
+    // If the user has onboarded, the Snaps Platform is considered ready,
+    // if it isn't forced to be disabled via feature flags.
+    const isReady = flags.disableSnaps !== true;
+    if (this.state.isReady !== isReady) {
+      this.update((state) => {
+        state.isReady = isReady;
+      });
+    }
+
     assert(
-      flags.disableSnaps !== true,
+      isReady,
       'The Snaps platform requires basic functionality to be used. Enable basic functionality in the settings to use the Snaps platform.',
     );
   }
@@ -1803,7 +1824,7 @@ export class SnapController extends BaseController<
    * @param snapId - The id of the Snap to start.
    */
   async startSnap(snapId: SnapId): Promise<void> {
-    await this.#assertCanUsePlatform();
+    await this.#ensureCanUsePlatform();
     const snap = this.state.snaps[snapId];
 
     if (!snap.enabled) {
@@ -2387,6 +2408,7 @@ export class SnapController extends BaseController<
     snapIds.forEach((snapId) => this.#revokeAllSnapPermissions(snapId));
 
     this.update((state) => {
+      state.isReady = false;
       state.snaps = {};
       state.snapStates = {};
       state.unencryptedSnapStates = {};
@@ -2703,7 +2725,7 @@ export class SnapController extends BaseController<
     origin: string,
     requestedSnaps: RequestSnapsParams,
   ): Promise<RequestSnapsResult> {
-    await this.#assertCanUsePlatform();
+    await this.#ensureCanUsePlatform();
 
     const result: RequestSnapsResult = {};
 
@@ -2989,7 +3011,7 @@ export class SnapController extends BaseController<
     if (!automaticUpdate) {
       this.#assertCanInstallSnaps();
     }
-    await this.#assertCanUsePlatform();
+    await this.#ensureCanUsePlatform();
 
     const snap = this.getExpect(snapId);
 
@@ -3624,7 +3646,7 @@ export class SnapController extends BaseController<
     handler: handlerType,
     request: rawRequest,
   }: SnapRpcHookArgs & { snapId: SnapId }): Promise<unknown> {
-    await this.#assertCanUsePlatform();
+    await this.#ensureCanUsePlatform();
 
     const snap = this.get(snapId);