diff --git a/packages/authenticated-user-storage/CHANGELOG.md b/packages/authenticated-user-storage/CHANGELOG.md
index 322a697481b..d1401d8ae9a 100644
--- a/packages/authenticated-user-storage/CHANGELOG.md
+++ b/packages/authenticated-user-storage/CHANGELOG.md
@@ -9,6 +9,8 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ### Changed
 
+- Route `setAssetsWatchlist` through `BaseDataService.executeMutation` so
+  watchlist writes are not cached, deduplicated, or retried.
 - Bump `@metamask/utils` from `^11.11.0` to `^11.12.0` ([#10076](https://github.com/MetaMask/core/pull/10076))
 
 ### Removed
diff --git a/packages/authenticated-user-storage/src/authenticated-user-storage-method-action-types.ts b/packages/authenticated-user-storage/src/authenticated-user-storage-method-action-types.ts
index 39c88ae9c5b..bf5202ea8ec 100644
--- a/packages/authenticated-user-storage/src/authenticated-user-storage-method-action-types.ts
+++ b/packages/authenticated-user-storage/src/authenticated-user-storage-method-action-types.ts
@@ -75,7 +75,8 @@ export type AuthenticatedUserStorageServiceGetAssetsWatchlistAction = {
  * contain at most `ASSETS_WATCHLIST_MAX_ASSETS` CAIP-19 asset identifiers;
  * this is enforced by `assertAssetsWatchlistBlobForWrite` before the
  * request is sent.
- * @param clientType - Optional client type header.
+ * @param clientTypeOrGlobalId - Optional client type header or mutation ID.
+ * @param globalId - Optional mutation ID when a client type is provided.
  * @throws A `StructError` from `@metamask/superstruct` if `blob` is
  * structurally invalid or `assets` exceeds the cap; an `HttpError` from
  * `@metamask/controller-utils` if the API responds with a non-2xx status.
diff --git a/packages/authenticated-user-storage/src/authenticated-user-storage.test.ts b/packages/authenticated-user-storage/src/authenticated-user-storage.test.ts
index f0c5c3ee8f8..88b9729c1ff 100644
--- a/packages/authenticated-user-storage/src/authenticated-user-storage.test.ts
+++ b/packages/authenticated-user-storage/src/authenticated-user-storage.test.ts
@@ -461,6 +461,59 @@ describe('AuthenticatedUserStorageService', () => {
 
       expect(mock.isDone()).toBe(true);
     });
+
+    it('does not retry a failed request', async () => {
+      nock(MOCK_ASSETS_WATCHLIST_URL)
+        .put('')
+        .reply(500, { error: 'server error' })
+        .put('')
+        .reply(200);
+      const { service } = createService();
+
+      await expect(
+        service.setAssetsWatchlist(MOCK_ASSETS_WATCHLIST_BLOB),
+      ).rejects.toThrow('Failed to put assets watchlist: 500');
+    });
+
+    it('does not deduplicate concurrent requests', async () => {
+      const scope = nock(MOCK_ASSETS_WATCHLIST_URL).put('').twice().reply(200);
+      const { service } = createService();
+
+      await Promise.all([
+        service.setAssetsWatchlist(MOCK_ASSETS_WATCHLIST_BLOB),
+        service.setAssetsWatchlist(MOCK_ASSETS_WATCHLIST_BLOB),
+      ]);
+
+      expect(scope.isDone()).toBe(true);
+    });
+
+    it('includes the global ID in mutation cache updates', async () => {
+      handleMockSetAssetsWatchlist();
+      const { service, messenger } = createService();
+      const publishSpy = jest.spyOn(messenger, 'publish');
+
+      await service.setAssetsWatchlist(MOCK_ASSETS_WATCHLIST_BLOB, 'global-id');
+
+      expect(publishSpy).toHaveBeenCalledWith(
+        expect.stringContaining(
+          'AuthenticatedUserStorageService:cacheUpdated:',
+        ),
+        expect.objectContaining({
+          objectType: 'mutation',
+          state: expect.objectContaining({
+            mutations: [
+              expect.objectContaining({
+                mutationKey: [
+                  'AuthenticatedUserStorageService:setAssetsWatchlist',
+                  MOCK_ASSETS_WATCHLIST_BLOB,
+                ],
+                meta: { globalId: 'global-id' },
+              }),
+            ],
+          }),
+        }),
+      );
+    });
   });
 
   describe('cache invalidation', () => {
diff --git a/packages/authenticated-user-storage/src/authenticated-user-storage.ts b/packages/authenticated-user-storage/src/authenticated-user-storage.ts
index 2b14522fe3c..989d909d238 100644
--- a/packages/authenticated-user-storage/src/authenticated-user-storage.ts
+++ b/packages/authenticated-user-storage/src/authenticated-user-storage.ts
@@ -34,6 +34,19 @@ import {
  */
 export const serviceName = 'AuthenticatedUserStorageService';
 
+/**
+ * Checks whether a value is a supported client type.
+ *
+ * This distinguishes the existing client-type argument from the optional
+ * mutation global ID when the method is invoked through a UI query client.
+ *
+ * @param value - The value to check.
+ * @returns Whether the value is a client type.
+ */
+function isClientType(value: string | undefined): value is ClientType {
+  return value === 'extension' || value === 'mobile' || value === 'portfolio';
+}
+
 /**
  * Builds the versioned API base URL for a given environment.
  *
@@ -392,23 +405,31 @@ export class AuthenticatedUserStorageService extends BaseDataService<
    * contain at most `ASSETS_WATCHLIST_MAX_ASSETS` CAIP-19 asset identifiers;
    * this is enforced by `assertAssetsWatchlistBlobForWrite` before the
    * request is sent.
-   * @param clientType - Optional client type header.
+   * @param clientTypeOrGlobalId - Optional client type header or mutation ID.
+   * @param globalId - Optional mutation ID when a client type is provided.
    * @throws A `StructError` from `@metamask/superstruct` if `blob` is
    * structurally invalid or `assets` exceeds the cap; an `HttpError` from
    * `@metamask/controller-utils` if the API responds with a non-2xx status.
    */
   async setAssetsWatchlist(
     blob: AssetsWatchlistBlob,
-    clientType?: ClientType,
+    clientTypeOrGlobalId?: ClientType | string,
+    globalId?: string,
   ): Promise<void> {
     assertAssetsWatchlistBlobForWrite(blob);
 
     const url = `${getAuthenticatedStorageUrl(this.#environment)}/preferences/assets-watchlist`;
-
-    await this.fetchQuery({
-      queryKey: [`${this.name}:setAssetsWatchlist`, blob as unknown as Json],
-      staleTime: 0,
-      queryFn: async () => {
+    const clientType = isClientType(clientTypeOrGlobalId)
+      ? clientTypeOrGlobalId
+      : undefined;
+    const mutationGlobalId = clientType
+      ? globalId
+      : (globalId ?? clientTypeOrGlobalId);
+
+    await this.executeMutation({
+      mutationKey: [`${this.name}:setAssetsWatchlist`, blob as Json],
+      globalId: mutationGlobalId,
+      mutationFn: async () => {
         const headers = await this.#getHeaders(clientType);
         const response = await fetch(url, {
           method: 'PUT',