diff --git a/packages/assets-controller/CHANGELOG.md b/packages/assets-controller/CHANGELOG.md
index b6ac2dd66d..8c69404c1d 100644
--- a/packages/assets-controller/CHANGELOG.md
+++ b/packages/assets-controller/CHANGELOG.md
@@ -23,6 +23,8 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ### Fixed
 
+- Run `RpcFallbackMiddleware` on Accounts API poll updates (`handleAssetsUpdate`), not only in the forced `getAssets` fast pipeline, so a stale amount for tokens omitted from poll responses no longer survives between forced refreshes while the wallet sits open ([#10078](https://github.com/MetaMask/core/pull/10078))
+  - WebSocket, RPC, and Snap updates are excluded: WebSocket pushes are incremental single-asset updates where absence is not staleness, and RPC/Snap updates must not re-trigger RPC
 - Fix stale balances shown right after a transaction confirms: the post-confirmation refresh now calls `getAssets` with `bypassServerCache: true`, since WebSocket events do not invalidate the Accounts API's server-side cache and a plain refetch within its 60s window returns the pre-transaction snapshot ([#10068](https://github.com/MetaMask/core/pull/10068))
 - Fix stale balances surviving in state when the Accounts API returns no entry for an asset it does not index (or reports an untrusted `0`), which the `merge` update kept as the previous amount ([#10061](https://github.com/MetaMask/core/pull/10061))
   - `RpcFallbackMiddleware` now re-reads EVM assets tracked in state (`assetsBalance` or `customAssets`) whose balance is empty in the current response, passing them to `RpcDataSource` as `customAssets`, in addition to its existing retry of chains in `response.errors`. Staking vault assets and assets on chains outside the request or the account's supported set are excluded.
diff --git a/packages/assets-controller/src/AssetsController.test.ts b/packages/assets-controller/src/AssetsController.test.ts
index 4c8a7e4c8f..4efe9e6257 100644
--- a/packages/assets-controller/src/AssetsController.test.ts
+++ b/packages/assets-controller/src/AssetsController.test.ts
@@ -23,6 +23,7 @@ import type {
 import type { AccountsApiDataSourceConfig } from './data-sources/AccountsApiDataSource.js';
 import type { PriceDataSourceConfig } from './data-sources/PriceDataSource.js';
 import { PriceDataSource } from './data-sources/PriceDataSource.js';
+import { RpcDataSource } from './data-sources/RpcDataSource.js';
 import { TokenDataSource } from './data-sources/TokenDataSource.js';
 import { buildDefaultAssetsInfo } from './defaults.js';
 import type { Assets3346MigrationState } from './migrations/healAssetsInfoMetadata.js';
@@ -1763,6 +1764,76 @@ describe('AssetsController', () => {
   });
 
   describe('handleAssetsUpdate', () => {
+    it('re-reads tracked assets an Accounts API poll left empty via the RPC fallback', async () => {
+      const initialState: Partial<AssetsControllerState> = {
+        assetsBalance: {
+          [MOCK_ACCOUNT_ID]: { [MOCK_ASSET_ID]: { amount: '1000' } },
+        },
+      };
+      const rpcMiddleware = jest.fn(
+        async (ctx: unknown, next: (ctx: unknown) => Promise<unknown>) =>
+          next(ctx),
+      );
+      const rpcMiddlewareGetter = jest
+        .spyOn(RpcDataSource.prototype, 'assetsMiddleware', 'get')
+        .mockReturnValue(rpcMiddleware as never);
+
+      await withController({ state: initialState }, async ({ controller }) => {
+        const pollRequest: DataRequest = {
+          accountsWithSupportedChains: [
+            {
+              account: createMockInternalAccount(),
+              supportedChains: ['eip155:1' as ChainId],
+            },
+          ],
+          chainIds: ['eip155:1' as ChainId],
+          dataTypes: ['balance'],
+        };
+
+        // The poll response omits MOCK_ASSET_ID even though state tracks it —
+        // the fallback must hand it to RPC for an on-chain re-read.
+        await controller.handleAssetsUpdate(
+          {
+            updateMode: 'merge',
+            assetsBalance: {
+              [MOCK_ACCOUNT_ID]: {
+                [MOCK_NATIVE_ASSET_ID]: { amount: '2' },
+              },
+            },
+          },
+          'AccountsApiDataSource',
+          pollRequest,
+        );
+
+        expect(rpcMiddleware).toHaveBeenCalledTimes(1);
+        const [rpcCtx] = rpcMiddleware.mock.calls[0] as [
+          { request: DataRequest },
+        ];
+        expect(rpcCtx.request.chainIds).toStrictEqual(['eip155:1']);
+        expect(rpcCtx.request.customAssets).toContain(MOCK_ASSET_ID);
+
+        // Same update from the WebSocket source must NOT trigger the
+        // fallback: its pushes are incremental single-asset updates, so an
+        // absent asset is not stale there.
+        rpcMiddleware.mockClear();
+        await controller.handleAssetsUpdate(
+          {
+            updateMode: 'merge',
+            assetsBalance: {
+              [MOCK_ACCOUNT_ID]: {
+                [MOCK_NATIVE_ASSET_ID]: { amount: '2' },
+              },
+            },
+          },
+          'AccountActivityDataSource',
+          pollRequest,
+        );
+        expect(rpcMiddleware).not.toHaveBeenCalled();
+      });
+
+      rpcMiddlewareGetter.mockRestore();
+    });
+
     it('does not fail when parent trace rejects after enrichment completes', async () => {
       const traceMock = jest
         .fn()
diff --git a/packages/assets-controller/src/AssetsController.ts b/packages/assets-controller/src/AssetsController.ts
index 46ae9495ff..a277f7ab3d 100644
--- a/packages/assets-controller/src/AssetsController.ts
+++ b/packages/assets-controller/src/AssetsController.ts
@@ -3912,6 +3912,7 @@ export class AssetsController extends BaseController<
           sourceId === 'AccountActivityDataSource' &&
           this.#isBasicFunctionality();
 
+        const shouldRunRpcFallback = sourceId === 'AccountsApiDataSource';
         const enrichmentSources: AssetsDataSource[] = [
           ...(shouldGraduateCustomAssets
             ? [this.#customAssetGraduationMiddleware]
@@ -3925,6 +3926,7 @@ export class AssetsController extends BaseController<
                 },
               ]
             : []),
+          ...(shouldRunRpcFallback ? [this.#rpcFallbackMiddleware] : []),
           this.#detectionMiddleware,
         ];
         if (this.#isBasicFunctionality()) {