diff --git a/packages/api/src/middleware/remoteAgentAuth.spec.ts b/packages/api/src/middleware/remoteAgentAuth.spec.ts
index 3e87378915..51c0164d28 100644
--- a/packages/api/src/middleware/remoteAgentAuth.spec.ts
+++ b/packages/api/src/middleware/remoteAgentAuth.spec.ts
@@ -53,7 +53,7 @@ import jwt from 'jsonwebtoken';
 import jwksRsa from 'jwks-rsa';
 import { SystemRoles } from 'librechat-data-provider';
 import { fetch as undiciFetch } from 'undici';
-import { logger, tenantStorage } from '@librechat/data-schemas';
+import { getTenantId, logger, tenantStorage } from '@librechat/data-schemas';
 import { clearRemoteAgentAuthCache, createRemoteAgentAuth } from './remoteAgentAuth';
 import { findOpenIDUser, getOpenIdEmail } from '../auth/openid';
 import { isEnabled, math } from '~/utils';
@@ -395,6 +395,45 @@ describe('createRemoteAgentAuth', () => {
       expect(mockNext).toHaveBeenCalled();
     });
 
+    it('restores tenant context from the API key user before continuing', async () => {
+      const deps = makeDeps(makeConfig({}, { enabled: true }));
+      const req = makeReq();
+      let observedTenantId: string | undefined;
+      const next = jest.fn(() => {
+        observedTenantId = getTenantId();
+      });
+      deps.apiKeyMiddleware.mockImplementation((request: unknown, _res: unknown, next) => {
+        (request as Request).user = makeUser({ tenantId: 'tenant-api-key' });
+        next();
+      });
+
+      await createRemoteAgentAuth(asDeps(deps))(req as Request, makeRes().res, next);
+
+      expect(observedTenantId).toBe('tenant-api-key');
+      expect(next).toHaveBeenCalledWith();
+    });
+
+    it('preserves pre-auth tenant context for a tenantless API key user', async () => {
+      const deps = makeDeps(makeConfig({}, { enabled: true }));
+      const req = makeReq();
+      let observedTenantId: string | undefined;
+      const next = jest.fn(() => {
+        observedTenantId = getTenantId();
+      });
+      deps.apiKeyMiddleware.mockImplementation((request: unknown, _res: unknown, next) => {
+        (request as Request).user = makeUser({ tenantId: undefined });
+        next();
+      });
+
+      await tenantStorage.run({ tenantId: 'tenant-preauth' }, async () => {
+        await createRemoteAgentAuth(asDeps(deps))(req as Request, makeRes().res, next);
+      });
+
+      expect(observedTenantId).toBe('tenant-preauth');
+      expect(req).toMatchObject({ tenantId: 'tenant-preauth' });
+      expect(next).toHaveBeenCalledWith();
+    });
+
     it('returns 401 when apiKey is disabled and no token present', async () => {
       const deps = makeDeps(makeConfig({}, { enabled: false }));
       const { res, status, json } = makeRes();
@@ -446,6 +485,67 @@ describe('createRemoteAgentAuth', () => {
       expect(deps.apiKeyMiddleware).not.toHaveBeenCalled();
     });
 
+    it('restores tenant context from the OIDC user before continuing', async () => {
+      setupOidcMocks({ sub: 'sub123', email: 'agent@test.com' });
+      const deps = makeDeps();
+      deps.findUser = makeFindUser(makeUser({ tenantId: 'tenant-oidc' }));
+      const req = makeReq({ authorization: `Bearer ${FAKE_TOKEN}` });
+      let observedTenantId: string | undefined;
+      const next = jest.fn(() => {
+        observedTenantId = getTenantId();
+      });
+
+      await createRemoteAgentAuth(asDeps(deps))(req as Request, makeRes().res, next);
+
+      expect(observedTenantId).toBe('tenant-oidc');
+      expect(next).toHaveBeenCalledWith();
+    });
+
+    it('preserves pre-auth tenant context for a tenantless OIDC user', async () => {
+      setupOidcMocks({ sub: 'sub123', email: 'agent@test.com' });
+      const deps = makeDeps();
+      const req = makeReq({ authorization: `Bearer ${FAKE_TOKEN}` });
+      let observedTenantId: string | undefined;
+      const next = jest.fn(() => {
+        observedTenantId = getTenantId();
+      });
+
+      await tenantStorage.run({ tenantId: 'tenant-preauth' }, async () => {
+        await createRemoteAgentAuth(asDeps(deps))(req as Request, makeRes().res, next);
+      });
+
+      expect(observedTenantId).toBe('tenant-preauth');
+      expect(req).toMatchObject({ tenantId: 'tenant-preauth' });
+      expect(next).toHaveBeenCalledWith();
+    });
+
+    it('rejects a tenant context that conflicts with the resolved OIDC user', async () => {
+      setupOidcMocks({ sub: 'sub123', email: 'agent@test.com' });
+      const deps = makeDeps();
+      deps.findUser = makeFindUser(
+        makeUser({
+          tenantId: 'tenant-user',
+          provider: undefined,
+          openidId: undefined,
+          openidIssuer: undefined,
+        }),
+      );
+      const { res, status, json } = makeRes();
+
+      await tenantStorage.run({ tenantId: 'tenant-request' }, async () => {
+        await createRemoteAgentAuth(asDeps(deps))(
+          makeReq({ authorization: `Bearer ${FAKE_TOKEN}` }) as Request,
+          res,
+          mockNext,
+        );
+      });
+
+      expect(status).toHaveBeenCalledWith(401);
+      expect(json).toHaveBeenCalledWith({ error: 'Unauthorized' });
+      expect(deps.updateUser).not.toHaveBeenCalled();
+      expect(mockNext).not.toHaveBeenCalled();
+    });
+
     it('re-evaluates OIDC auth config after resolving the user tenant', async () => {
       setupOidcMocks({ sub: 'sub123', email: 'agent@test.com', scope: 'remote_agent' });
       const deps = makeDeps();
diff --git a/packages/api/src/middleware/remoteAgentAuth.ts b/packages/api/src/middleware/remoteAgentAuth.ts
index c198292dc2..5aaaf951c3 100644
--- a/packages/api/src/middleware/remoteAgentAuth.ts
+++ b/packages/api/src/middleware/remoteAgentAuth.ts
@@ -9,6 +9,8 @@ import type { Algorithm, JwtPayload, VerifyOptions } from 'jsonwebtoken';
 import type { TAgentsEndpoint } from 'librechat-data-provider';
 import type { RequestInit } from 'undici';
 import type { GetAppConfigOptions } from '../app/service';
+import type { ServerRequest } from '~/types/http';
+import type { ContextRequest } from './tenant';
 import {
   getLibreChatRolesForOpenIdSync,
   getOpenIdRolesForOpenIdSync,
@@ -17,6 +19,7 @@ import {
 } from '../auth/openidRoleSync';
 import { findOpenIDUser, getOpenIdEmail, normalizeOpenIdIssuer } from '../auth/openid';
 import { getEnvProxyDispatcher, getHttpsProxyAgent } from '~/utils/proxy';
+import { tenantContextMiddleware } from './tenant';
 import { isEnabled, math } from '~/utils';
 
 export interface RemoteAgentAuthDeps {
@@ -293,12 +296,50 @@ function isApiKeyEnabled(config: AppConfig): boolean {
   return getRemoteAuthConfig(config)?.apiKey?.enabled !== false;
 }
 
+function rejectTenantContextConflict(
+  requestTenantId: string | undefined,
+  userTenantId: string | undefined,
+  res: Response,
+): boolean {
+  if (!requestTenantId || !userTenantId || requestTenantId === userTenantId) {
+    return false;
+  }
+
+  logger.warn('[remoteAgentAuth] Authenticated user tenant conflicts with request tenant context');
+  res.status(401).json({ error: 'Unauthorized' });
+  return true;
+}
+
+function continueWithAuthenticatedTenantContext(
+  req: Request,
+  res: Response,
+  next: NextFunction,
+): void {
+  const requestTenantId = getTenantId();
+  const userTenantId = (req.user as { tenantId?: string } | undefined)?.tenantId;
+
+  if (rejectTenantContextConflict(requestTenantId, userTenantId, res)) {
+    return;
+  }
+
+  const contextRequest = req as ContextRequest;
+  if (requestTenantId) {
+    contextRequest.tenantId = requestTenantId;
+  }
+  tenantContextMiddleware(req as ServerRequest, res, next);
+}
+
 async function enforceApiKeyTenantPolicy(
   req: Request,
   res: Response,
   next: NextFunction,
   getAppConfig: RemoteAgentAuthDeps['getAppConfig'],
 ): Promise<void> {
+  const userTenantId = (req.user as { tenantId?: string } | undefined)?.tenantId;
+  if (rejectTenantContextConflict(getTenantId(), userTenantId, res)) {
+    return;
+  }
+
   const config = await getAppConfig(getConfigOptions(req));
 
   if (!isApiKeyEnabled(config)) {
@@ -307,7 +348,7 @@ async function enforceApiKeyTenantPolicy(
     return;
   }
 
-  next();
+  continueWithAuthenticatedTenantContext(req, res, next);
 }
 
 async function runApiKeyAuth(
@@ -648,6 +689,10 @@ export function createRemoteAgentAuth({
         return;
       }
 
+      if (rejectTenantContextConflict(getTenantId(), userResolution.user.tenantId, res)) {
+        return;
+      }
+
       if (
         !(await enforceOidcTenantPolicy(
           token,
@@ -687,7 +732,7 @@ export function createRemoteAgentAuth({
       await updateResolvedUser(userResolution, updateUser);
 
       req.user = userResolution.user;
-      return next();
+      return continueWithAuthenticatedTenantContext(req, res, next);
     } catch (err) {
       logger.error('[remoteAgentAuth] Unexpected error', err);
       res.status(500).json({ error: 'Internal server error' });