diff --git a/apps/desktop/src/app/chat/composer/hooks/use-composer-queue.ts b/apps/desktop/src/app/chat/composer/hooks/use-composer-queue.ts
index 9d54e17bd957..8912bab778af 100644
--- a/apps/desktop/src/app/chat/composer/hooks/use-composer-queue.ts
+++ b/apps/desktop/src/app/chat/composer/hooks/use-composer-queue.ts
@@ -34,6 +34,7 @@ interface UseComposerQueueArgs {
   onCancel: ChatBarProps['onCancel']
   onSubmit: ChatBarProps['onSubmit']
   queueEditRef: RefObject<QueueEditState | null>
+  queueProfile?: string | null
   queueSessionKey: ChatBarProps['queueSessionKey']
   sessionId: string | null | undefined
 }
@@ -58,6 +59,7 @@ export function useComposerQueue({
   onCancel,
   onSubmit,
   queueEditRef,
+  queueProfile,
   queueSessionKey,
   sessionId
 }: UseComposerQueueArgs) {
@@ -171,7 +173,7 @@ export function useComposerQueue({
       return false
     }
 
-    if (!enqueueQueuedPrompt(activeQueueSessionKey, { text, attachments })) {
+    if (!enqueueQueuedPrompt(activeQueueSessionKey, { text, attachments, profile: queueProfile })) {
       return false
     }
 
@@ -180,7 +182,7 @@ export function useComposerQueue({
     triggerHaptic('selection')
 
     return true
-  }, [activeQueueSessionKey, attachments, clearDraft, draftRef, scope.attachments])
+  }, [activeQueueSessionKey, attachments, clearDraft, draftRef, queueProfile, scope.attachments])
 
   // All queue drain paths share one lock + send-then-remove sequence.
   // `pickEntry` lets each caller choose head, by-id, or skip-edited.
@@ -205,6 +207,7 @@ export function useComposerQueue({
           onSubmit(entry.text, {
             attachments: entry.attachments,
             fromQueue: true,
+            ...(entry.profile ? { profile: entry.profile } : {}),
             sessionId: drainRuntimeSessionId,
             storedSessionId: drainQueueSessionKey
           })
diff --git a/apps/desktop/src/app/chat/composer/index.tsx b/apps/desktop/src/app/chat/composer/index.tsx
index ce0e43d7d1cc..79f9f29905d0 100644
--- a/apps/desktop/src/app/chat/composer/index.tsx
+++ b/apps/desktop/src/app/chat/composer/index.tsx
@@ -68,6 +68,7 @@ export function ChatBar({
   focusKey,
   gateway,
   maxRecordingSeconds = 120,
+  queueProfile,
   queueSessionKey,
   sessionId,
   state,
@@ -203,6 +204,7 @@ export function ChatBar({
     onCancel,
     onSubmit,
     queueEditRef,
+    queueProfile,
     queueSessionKey,
     sessionId
   })
diff --git a/apps/desktop/src/app/chat/composer/types.ts b/apps/desktop/src/app/chat/composer/types.ts
index 24abcf373697..3d70ed8a49d4 100644
--- a/apps/desktop/src/app/chat/composer/types.ts
+++ b/apps/desktop/src/app/chat/composer/types.ts
@@ -38,6 +38,7 @@ export interface ChatBarProps {
   maxRecordingSeconds?: number
   state: ChatBarState
   gateway?: HermesGateway | null
+  queueProfile?: string | null
   queueSessionKey?: string | null
   sessionId?: string | null
   cwd?: string | null
diff --git a/apps/desktop/src/app/chat/index.tsx b/apps/desktop/src/app/chat/index.tsx
index b47f0dfa9907..c9bc2676fd51 100644
--- a/apps/desktop/src/app/chat/index.tsx
+++ b/apps/desktop/src/app/chat/index.tsx
@@ -276,6 +276,11 @@ export function ChatView({
   const messagesEmpty = useStore(view.$messagesEmpty)
   const lastVisibleIsUser = useStore(view.$lastVisibleIsUser)
   const selectedSessionId = useStore(view.$storedId)
+
+  const queueProfile = selectedSessionId
+    ? ($sessions.get().find(session => sessionMatchesStoredId(session, selectedSessionId))?.profile ?? null)
+    : null
+
   const resumeExhaustedSessionId = useStore($resumeExhaustedSessionId)
   // A tile IS its session — no route involved, never "mismatched".
   const routedSessionId = isPrimary ? routeSessionId(location.pathname) : selectedSessionId
@@ -524,6 +529,7 @@ export function ChatView({
               onSteer={onSteer}
               onSubmit={onSubmit}
               onTranscribeAudio={onTranscribeAudio}
+              queueProfile={queueProfile}
               queueSessionKey={selectedSessionId}
               sessionId={activeSessionId}
               state={chatBarState}
diff --git a/apps/desktop/src/app/chat/session-tile-actions.ts b/apps/desktop/src/app/chat/session-tile-actions.ts
index 4eca47f5c094..2d54a7f08675 100644
--- a/apps/desktop/src/app/chat/session-tile-actions.ts
+++ b/apps/desktop/src/app/chat/session-tile-actions.ts
@@ -41,7 +41,7 @@ import {
   runRewindSubmit
 } from '../session/hooks/use-prompt-actions/rewind'
 import { useSubmitPrompt } from '../session/hooks/use-prompt-actions/submit'
-import { type SubmitTextOptions } from '../session/hooks/use-prompt-actions/utils'
+import { type GatewayRequest, type SubmitTextOptions } from '../session/hooks/use-prompt-actions/utils'
 
 import type { ComposerScope } from './composer/scope'
 
@@ -54,7 +54,7 @@ interface SessionTileActionsArgs {
 export function useSessionTileActions({ runtimeId, scope, storedSessionId }: SessionTileActionsArgs) {
   const { t } = useI18n()
   const copy = t.desktop
-  const { requestGateway } = useGatewayRequest()
+  const { requestGateway, requestGatewayForProfile } = useGatewayRequest()
 
   const runtimeIdRef = useRef(runtimeId)
   runtimeIdRef.current = runtimeId
@@ -95,9 +95,15 @@ export function useSessionTileActions({ runtimeId, scope, storedSessionId }: Ses
     async (
       sessionId: string,
       attachments: ComposerAttachment[],
-      options: { updateComposerAttachments?: boolean } = {}
+      options: { profile?: string | null; requestGateway?: GatewayRequest; updateComposerAttachments?: boolean } = {}
     ): Promise<ComposerAttachment[]> => {
-      const remote = $connection.get()?.mode === 'remote'
+      const attachmentGateway = options.requestGateway ?? requestGateway
+
+      const profileConnection = options.profile
+        ? await window.hermesDesktop?.getConnection(options.profile).catch(() => null)
+        : null
+
+      const remote = (profileConnection ?? $connection.get())?.mode === 'remote'
       const synced: ComposerAttachment[] = []
 
       for (const attachment of attachments) {
@@ -108,7 +114,11 @@ export function useSessionTileActions({ runtimeId, scope, storedSessionId }: Ses
         }
 
         if (attachment.kind === 'image' || attachment.kind === 'file') {
-          const next = await uploadComposerAttachment(attachment, { remote, requestGateway, sessionId })
+          const next = await uploadComposerAttachment(attachment, {
+            remote,
+            requestGateway: attachmentGateway,
+            sessionId
+          })
 
           if (options.updateComposerAttachments ?? true) {
             scope.attachments.update(next)
@@ -140,6 +150,7 @@ export function useSessionTileActions({ runtimeId, scope, storedSessionId }: Ses
     // token is a stable constant (the guard never trips for a tile).
     getRouteToken: () => runtimeId,
     requestGateway,
+    requestGatewayForProfile,
     // Tile ids are always bound before this hook mounts, so routed recovery is
     // unreachable here; keep the shared submit contract explicit.
     resumeStoredSession: () => undefined,
diff --git a/apps/desktop/src/app/contrib/wiring.tsx b/apps/desktop/src/app/contrib/wiring.tsx
index f47a2301b2ac..193afd147112 100644
--- a/apps/desktop/src/app/contrib/wiring.tsx
+++ b/apps/desktop/src/app/contrib/wiring.tsx
@@ -197,7 +197,7 @@ export function ContribWiring({ children }: { children: ReactNode }) {
     setMessages
   })
 
-  const { connectionRef, gatewayRef, requestGateway } = useGatewayRequest()
+  const { connectionRef, gatewayRef, requestGateway, requestGatewayForProfile } = useGatewayRequest()
 
   const {
     loadMoreMessagingForPlatform,
@@ -530,6 +530,7 @@ export function ContribWiring({ children }: { children: ReactNode }) {
     openMemoryGraph: openStarmap,
     refreshSessions,
     requestGateway,
+    requestGatewayForProfile,
     resumeStoredSession: resumeSession,
     selectedStoredSessionIdRef,
     startFreshSessionDraft,
@@ -539,8 +540,17 @@ export function ContribWiring({ children }: { children: ReactNode }) {
 
   // Runs outside the selected ChatBar so queues belonging to background
   // sessions continue once those sessions are idle.
+  const getProfileForStoredSession = useCallback((storedSessionId: string): null | string => {
+    const stored = [...$sessions.get(), ...$messagingSessions.get()].find(session =>
+      sessionMatchesStoredId(session, storedSessionId)
+    )
+
+    return stored?.profile ?? null
+  }, [])
+
   useBackgroundQueueDrain({
     enabled: gatewayState === 'open',
+    getProfileForStoredSession,
     runtimeIdByStoredSessionIdRef,
     selectedStoredSessionId,
     submitText
diff --git a/apps/desktop/src/app/gateway/hooks/use-gateway-request.ts b/apps/desktop/src/app/gateway/hooks/use-gateway-request.ts
index d6c9ab0e029b..c5290bd4d4d7 100644
--- a/apps/desktop/src/app/gateway/hooks/use-gateway-request.ts
+++ b/apps/desktop/src/app/gateway/hooks/use-gateway-request.ts
@@ -3,7 +3,7 @@ import { useStore } from '@nanostores/react'
 import { useCallback, useEffect, useRef } from 'react'
 
 import type { HermesGateway } from '@/hermes'
-import { $gateway, ensureActiveGatewayOpen, isActivePrimary } from '@/store/gateway'
+import { $gateway, ensureActiveGatewayOpen, ensureGatewayOpenForProfile, isActivePrimary } from '@/store/gateway'
 import { $activeGatewayProfile } from '@/store/profile'
 import { $gatewayState, setConnection } from '@/store/session'
 
@@ -134,5 +134,18 @@ export function useGatewayRequest() {
     [ensureGatewayOpen]
   )
 
-  return { connectionRef, gatewayRef, requestGateway }
+  const requestGatewayForProfile = useCallback(
+    async <T>(profile: string, method: string, params: Record<string, unknown> = {}, timeoutMs?: number) => {
+      const gateway = await ensureGatewayOpenForProfile(profile)
+
+      if (!gateway) {
+        throw new Error(`Hermes gateway unavailable for profile: ${profile}`)
+      }
+
+      return gateway.request<T>(method, params, timeoutMs)
+    },
+    []
+  )
+
+  return { connectionRef, gatewayRef, requestGateway, requestGatewayForProfile }
 }
diff --git a/apps/desktop/src/app/session/hooks/use-background-queue-drain.test.tsx b/apps/desktop/src/app/session/hooks/use-background-queue-drain.test.tsx
index 9f5589b816f4..f8ed7b9d4ed6 100644
--- a/apps/desktop/src/app/session/hooks/use-background-queue-drain.test.tsx
+++ b/apps/desktop/src/app/session/hooks/use-background-queue-drain.test.tsx
@@ -11,17 +11,20 @@ import type { SubmitTextOptions } from './use-prompt-actions/utils'
 
 function Harness({
   enabled = true,
+  getProfileForStoredSession,
   runtimeMap,
   selectedStoredSessionId = 'stored-session-b',
   submitText
 }: {
   enabled?: boolean
+  getProfileForStoredSession?: (storedSessionId: string) => null | string
   runtimeMap: MutableRefObject<Map<string, string>>
   selectedStoredSessionId?: string | null
   submitText: (text: string, options?: SubmitTextOptions) => Promise<boolean> | boolean
 }) {
   useBackgroundQueueDrain({
     enabled,
+    getProfileForStoredSession,
     runtimeIdByStoredSessionIdRef: runtimeMap,
     selectedStoredSessionId,
     submitText
@@ -100,14 +103,25 @@ describe('useBackgroundQueueDrain', () => {
     const runtimeMap = { current: new Map<string, string>() }
     const submitText = vi.fn(async () => true)
 
-    enqueueQueuedPrompt('stored-session-a', { text: 'resume then send', attachments: [] })
+    enqueueQueuedPrompt('stored-session-a', {
+      text: 'resume then send',
+      attachments: [],
+      profile: 'persisted-background-profile'
+    })
 
-    render(<Harness runtimeMap={runtimeMap} submitText={submitText} />)
+    render(
+      <Harness
+        getProfileForStoredSession={() => 'stale-fallback-profile'}
+        runtimeMap={runtimeMap}
+        submitText={submitText}
+      />
+    )
 
     await waitFor(() => {
       expect(submitText).toHaveBeenCalledWith('resume then send', {
         attachments: [],
         fromQueue: true,
+        profile: 'persisted-background-profile',
         sessionId: null,
         storedSessionId: 'stored-session-a'
       })
diff --git a/apps/desktop/src/app/session/hooks/use-background-queue-drain.ts b/apps/desktop/src/app/session/hooks/use-background-queue-drain.ts
index 8d98df149313..c86c1ffe3707 100644
--- a/apps/desktop/src/app/session/hooks/use-background-queue-drain.ts
+++ b/apps/desktop/src/app/session/hooks/use-background-queue-drain.ts
@@ -20,6 +20,7 @@ type SubmitQueuedPrompt = (text: string, options?: SubmitTextOptions) => Promise
 
 interface BackgroundQueueDrainOptions {
   enabled: boolean
+  getProfileForStoredSession?: (storedSessionId: string) => null | string
   runtimeIdByStoredSessionIdRef: MutableRefObject<Map<string, string>>
   selectedStoredSessionId: string | null
   submitText: SubmitQueuedPrompt
@@ -37,6 +38,7 @@ const BACKGROUND_DRAIN_RETRY_MS = 750
  */
 export function useBackgroundQueueDrain({
   enabled,
+  getProfileForStoredSession,
   runtimeIdByStoredSessionIdRef,
   selectedStoredSessionId,
   submitText
@@ -113,11 +115,13 @@ export function useBackgroundQueueDrain({
           }
 
           const runtimeSessionId = runtimeIdByStoredSessionIdRef.current.get(sessionKey) ?? null
+          const profile = liveEntry.profile?.trim() || getProfileForStoredSession?.(sessionKey)?.trim() || null
 
           const accepted = await Promise.resolve(
             submitTextRef.current(liveEntry.text, {
               attachments: liveEntry.attachments,
               fromQueue: true,
+              ...(profile ? { profile } : {}),
               sessionId: runtimeSessionId,
               storedSessionId: sessionKey
             })
@@ -143,7 +147,7 @@ export function useBackgroundQueueDrain({
           drainingSessionIdsRef.current.delete(sessionKey)
         })
     },
-    [runtimeIdByStoredSessionIdRef, scheduleRetry, t]
+    [getProfileForStoredSession, runtimeIdByStoredSessionIdRef, scheduleRetry, t]
   )
 
   useEffect(() => {
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
index a06ee1294c08..ddc0001b3d44 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
@@ -77,6 +77,7 @@ function Harness({
   openMemoryGraph,
   refreshSessions,
   requestGateway,
+  requestGatewayForProfile,
   resumeStoredSession,
   seedMessages,
   selectedStoredSessionIdRef: selectedStoredSessionIdRefProp,
@@ -99,6 +100,12 @@ function Harness({
   openMemoryGraph?: () => void
   refreshSessions: () => Promise<void>
   requestGateway: <T>(method: string, params?: Record<string, unknown>) => Promise<T>
+  requestGatewayForProfile?: <T>(
+    profile: string,
+    method: string,
+    params?: Record<string, unknown>,
+    timeoutMs?: number
+  ) => Promise<T>
   resumeStoredSession?: (storedSessionId: string) => Promise<void> | void
   seedMessages?: unknown[]
   selectedStoredSessionIdRef?: MutableRefObject<string | null>
@@ -138,6 +145,7 @@ function Harness({
     openMemoryGraph: openMemoryGraph ?? (() => undefined),
     refreshSessions,
     requestGateway,
+    requestGatewayForProfile: requestGatewayForProfile ?? ((_, method, params) => requestGateway(method, params)),
     resumeStoredSession: resumeStoredSession ?? (() => undefined),
     selectedStoredSessionIdRef,
     startFreshSessionDraft: () => undefined,
@@ -601,6 +609,71 @@ describe('usePromptActions submit / queue drain semantics', () => {
     expect($busy.get()).toBe(false)
   })
 
+  it('a background queue drain with no runtime id resumes its stored session instead of using the foreground runtime', async () => {
+    $busy.set(false)
+
+    const calls: { method: string; params?: Record<string, unknown>; profile: string }[] = []
+    const recoveredBackgroundRuntimeId = 'rt-background-recovered'
+    const backgroundStoredSessionId = 'stored-background'
+    const backgroundProfile = 'background-profile'
+    const foregroundStoredSessionId = 'stored-foreground'
+    const resumeStoredSession = vi.fn()
+
+    const requestGateway = vi.fn(async () => {
+      throw new Error('foreground gateway must not serve a background-profile queue')
+    })
+
+    const requestGatewayForProfile = vi.fn(
+      async (profile: string, method: string, params?: Record<string, unknown>) => {
+        calls.push({ method, params, profile })
+
+        if (method === 'session.resume') {
+          return { session_id: recoveredBackgroundRuntimeId } as never
+        }
+
+        return {} as never
+      }
+    )
+
+    let handle: HarnessHandle | null = null
+    await actRender(
+      <Harness
+        getRoutedStoredSessionId={() => foregroundStoredSessionId}
+        getRuntimeIdForStoredSession={() => null}
+        onReady={h => (handle = h)}
+        refreshSessions={async () => undefined}
+        requestGateway={requestGateway}
+        requestGatewayForProfile={requestGatewayForProfile}
+        resumeStoredSession={resumeStoredSession}
+        storedSessionId={foregroundStoredSessionId}
+      />
+    )
+
+    const accepted = await handle!.submitText('resume queued background session', {
+      fromQueue: true,
+      profile: backgroundProfile,
+      sessionId: null,
+      storedSessionId: backgroundStoredSessionId
+    })
+
+    expect(accepted).toBe(true)
+    expect(calls).toEqual([
+      {
+        method: 'session.resume',
+        params: { session_id: backgroundStoredSessionId, source: 'desktop' },
+        profile: backgroundProfile
+      },
+      {
+        method: 'prompt.submit',
+        params: { session_id: recoveredBackgroundRuntimeId, text: 'resume queued background session' },
+        profile: backgroundProfile
+      }
+    ])
+    expect(requestGateway).not.toHaveBeenCalled()
+    expect(resumeStoredSession).not.toHaveBeenCalled()
+    expect(handle!.activeSessionIdRef.current).toBe(RUNTIME_SESSION_ID)
+  })
+
   it('a rejected fromQueue drain returns false (entry stays queued) and a later retry sends it', async () => {
     // A stale-session 404 must not strand the queued entry: submitPrompt returns
     // false on failure so the composer keeps it, and the edge-independent
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
index 1fde9070d4a3..c5eb80b6641e 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
@@ -179,6 +179,12 @@ interface PromptActionsOptions {
   openMemoryGraph: () => void
   refreshSessions: () => Promise<void>
   requestGateway: <T>(method: string, params?: Record<string, unknown>, timeoutMs?: number) => Promise<T>
+  requestGatewayForProfile: <T>(
+    profile: string,
+    method: string,
+    params?: Record<string, unknown>,
+    timeoutMs?: number
+  ) => Promise<T>
   resumeStoredSession: (storedSessionId: string) => Promise<void> | void
   selectedStoredSessionIdRef: MutableRefObject<string | null>
   startFreshSessionDraft: () => void
@@ -210,6 +216,7 @@ export function usePromptActions({
   openMemoryGraph,
   refreshSessions,
   requestGateway,
+  requestGatewayForProfile,
   resumeStoredSession,
   selectedStoredSessionIdRef,
   startFreshSessionDraft,
@@ -259,10 +266,16 @@ export function usePromptActions({
     async (
       sessionId: string,
       attachments: ComposerAttachment[],
-      options: { updateComposerAttachments?: boolean } = {}
+      options: { profile?: string | null; requestGateway?: GatewayRequest; updateComposerAttachments?: boolean } = {}
     ): Promise<ComposerAttachment[]> => {
+      const attachmentGateway = options.requestGateway ?? requestGateway
       const updateComposerAttachments = options.updateComposerAttachments ?? true
-      const remote = $connection.get()?.mode === 'remote'
+
+      const profileConnection = options.profile
+        ? await window.hermesDesktop?.getConnection(options.profile).catch(() => null)
+        : null
+
+      const remote = (profileConnection ?? $connection.get())?.mode === 'remote'
       const synced: ComposerAttachment[] = []
 
       for (const original of attachments) {
@@ -290,7 +303,11 @@ export function usePromptActions({
         }
 
         if (attachment.kind === 'image' || attachment.kind === 'file') {
-          const nextAttachment = await uploadComposerAttachment(attachment, { remote, requestGateway, sessionId })
+          const nextAttachment = await uploadComposerAttachment(attachment, {
+            remote,
+            requestGateway: attachmentGateway,
+            sessionId
+          })
 
           // Update-only: never resurrect a chip the user removed mid-upload.
           if (updateComposerAttachments) {
@@ -377,6 +394,7 @@ export function usePromptActions({
     getRuntimeIdForStoredSession,
     getRouteToken,
     requestGateway,
+    requestGatewayForProfile,
     resumeStoredSession,
     selectedStoredSessionIdRef,
     syncAttachmentsForSubmit,
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts b/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
index 709652dce7bf..c5a3ea0af069 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
@@ -39,12 +39,18 @@ interface SubmitPromptDeps {
   getRuntimeIdForStoredSession: (storedSessionId: string) => null | string
   getRouteToken: () => string
   requestGateway: GatewayRequest
+  requestGatewayForProfile: <T>(
+    profile: string,
+    method: string,
+    params?: Record<string, unknown>,
+    timeoutMs?: number
+  ) => Promise<T>
   resumeStoredSession: (storedSessionId: string) => Promise<void> | void
   selectedStoredSessionIdRef: MutableRefObject<string | null>
   syncAttachmentsForSubmit: (
     sessionId: string,
     attachments: ComposerAttachment[],
-    options?: { updateComposerAttachments?: boolean }
+    options?: { profile?: string | null; requestGateway?: GatewayRequest; updateComposerAttachments?: boolean }
   ) => Promise<ComposerAttachment[]>
   updateSessionState: (
     sessionId: string,
@@ -84,6 +90,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
     getRuntimeIdForStoredSession,
     getRouteToken,
     requestGateway,
+    requestGatewayForProfile,
     resumeStoredSession,
     selectedStoredSessionIdRef,
     syncAttachmentsForSubmit,
@@ -145,11 +152,23 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
       // must never inherit the currently selected session after the user moves
       // to another chat.
       const targetStoredSessionId = options?.storedSessionId ?? selectedStoredSessionIdRef.current
+      const targetProfile = options?.profile?.trim() || null
+
+      const targetRequestGateway: GatewayRequest = targetProfile
+        ? (method, params, timeoutMs) => requestGatewayForProfile(targetProfile, method, params, timeoutMs)
+        : requestGateway
 
       const targetStartedInCurrentView =
         !targetStoredSessionId || targetStoredSessionId === selectedStoredSessionIdRef.current
 
-      let sessionId: null | string = options?.sessionId ?? activeSessionIdRef.current
+      // An explicit null is authoritative: background drains use it to mean
+      // "no runtime mapping — resume storedSessionId". Only an omitted runtime
+      // target may inherit or recover the foreground session.
+      const inheritsForegroundRuntime = options?.sessionId === undefined
+
+      let sessionId: null | string = inheritsForegroundRuntime
+        ? activeSessionIdRef.current
+        : (options?.sessionId ?? null)
 
       // Pin the foreground session context for the whole async submit pipeline.
       // Without this, a fast session switch during session.resume / file.attach
@@ -295,8 +314,9 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
       // A route whose selected/runtime binding is incomplete or cross-wired
       // outranks a stale render-time runtime id (often from the previous
       // profile): force the full routed resume path below. An explicit queued
-      // runtime id (background drain) is authoritative and is left untouched.
-      if (!options?.sessionId && routedSessionNeedsResume) {
+      // runtime target — including null, which means resume its stored id — is
+      // authoritative and is left untouched.
+      if (inheritsForegroundRuntime && routedSessionNeedsResume) {
         sessionId = null
       }
 
@@ -306,7 +326,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         scope.setMessages(current => [...current, buildUserMessage()])
       }
 
-      if (!sessionId && routedStoredSessionId && routedSessionNeedsResume) {
+      if (inheritsForegroundRuntime && !sessionId && routedStoredSessionId && routedSessionNeedsResume) {
         // The URL still names a durable conversation, but a profile
         // swap/reconnect left its volatile session binding incomplete or
         // cross-wired. Run the full profile-aware resume path. Creating here
@@ -346,7 +366,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         // background queue drain only has the durable id). Continue that target
         // conversation; only a genuine new-chat draft may create a new session.
         try {
-          const resumed = await requestGateway<{ session_id: string }>('session.resume', {
+          const resumed = await targetRequestGateway<{ session_id: string }>('session.resume', {
             session_id: targetStoredSessionId,
             source: 'desktop'
           })
@@ -436,6 +456,8 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
 
       try {
         const syncedAttachments = await syncAttachmentsForSubmit(sessionId, attachments, {
+          profile: targetProfile,
+          requestGateway: targetRequestGateway,
           updateComposerAttachments: usingComposerAttachments
         })
 
@@ -457,7 +479,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
 
         try {
           await withSessionBusyRetry(() =>
-            requestGateway('prompt.submit', { session_id: sessionId, text }, PROMPT_SUBMIT_REQUEST_TIMEOUT_MS)
+            targetRequestGateway('prompt.submit', { session_id: sessionId, text }, PROMPT_SUBMIT_REQUEST_TIMEOUT_MS)
           )
         } catch (firstErr) {
           const recoverStoredSessionId = targetStoredSessionId ?? selectedStoredSessionIdRef.current
@@ -468,7 +490,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
             // backend loop (#55578 symptom d) rejects the submit even though
             // the stored session is fine — resume + retry instead of erroring
             // out and losing the session binding.
-            const resumed = await requestGateway<{ session_id: string }>('session.resume', {
+            const resumed = await targetRequestGateway<{ session_id: string }>('session.resume', {
               session_id: recoverStoredSessionId,
               source: 'desktop'
             })
@@ -485,7 +507,11 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
               }
 
               await withSessionBusyRetry(() =>
-                requestGateway('prompt.submit', { session_id: recoveredId, text }, PROMPT_SUBMIT_REQUEST_TIMEOUT_MS)
+                targetRequestGateway(
+                  'prompt.submit',
+                  { session_id: recoveredId, text },
+                  PROMPT_SUBMIT_REQUEST_TIMEOUT_MS
+                )
               )
             } else {
               submitErr = firstErr
@@ -564,6 +590,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
       getRuntimeIdForStoredSession,
       getRouteToken,
       requestGateway,
+      requestGatewayForProfile,
       resumeStoredSession,
       scope,
       selectedStoredSessionIdRef,
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/utils.ts b/apps/desktop/src/app/session/hooks/use-prompt-actions/utils.ts
index b1d41893cca6..6dae204b5634 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/utils.ts
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/utils.ts
@@ -226,6 +226,10 @@ export function visibleUserIndexAtOrdinal(messages: readonly ChatMessage[], targ
 export interface SubmitTextOptions {
   attachments?: ComposerAttachment[]
   fromQueue?: boolean
+  /** Owning profile for an offscreen queued session. When present, every RPC
+   *  in the submit pipeline uses that profile's background gateway without
+   *  activating it in the foreground. */
+  profile?: string | null
   /** Runtime session id to submit into. Queue drains pass this so a
    *  backgrounded/source session cannot be replaced by the current foreground
    *  session between enqueue and drain. */
diff --git a/apps/desktop/src/store/composer-queue.test.ts b/apps/desktop/src/store/composer-queue.test.ts
index 8012e2870f06..0b2853a746b7 100644
--- a/apps/desktop/src/store/composer-queue.test.ts
+++ b/apps/desktop/src/store/composer-queue.test.ts
@@ -51,6 +51,19 @@ describe('composer queue store', () => {
     expect(getQueuedPrompts(SESSION_KEY)[0]?.attachments[0]).not.toBe(source[0])
   })
 
+  it('persists the owning profile with queued prompts', () => {
+    enqueueQueuedPrompt(SESSION_KEY, { attachments: [], profile: ' work ', text: 'profiled' })
+
+    expect(getQueuedPrompts(SESSION_KEY)[0]?.profile).toBe('work')
+
+    const raw = JSON.parse(String(window.localStorage.getItem(QUEUE_STORAGE_KEY))) as Record<
+      string,
+      { profile?: string }[]
+    >
+
+    expect(raw[SESSION_KEY]?.[0]?.profile).toBe('work')
+  })
+
   it('updates and removes queued entries by id', () => {
     const first = enqueueQueuedPrompt(SESSION_KEY, { attachments: [], text: 'draft one' })
     const second = enqueueQueuedPrompt(SESSION_KEY, { attachments: [], text: 'draft two' })
diff --git a/apps/desktop/src/store/composer-queue.ts b/apps/desktop/src/store/composer-queue.ts
index 922e990fdce7..ccd5bf6f79e2 100644
--- a/apps/desktop/src/store/composer-queue.ts
+++ b/apps/desktop/src/store/composer-queue.ts
@@ -6,6 +6,7 @@ export interface QueuedPromptEntry {
   id: string
   text: string
   attachments: ComposerAttachment[]
+  profile?: string
   queuedAt: number
 }
 
@@ -80,7 +81,7 @@ export const getQueuedPrompts = (key: string | null | undefined): QueuedPromptEn
 
 export const enqueueQueuedPrompt = (
   key: string | null | undefined,
-  payload: { text: string; attachments: ComposerAttachment[] }
+  payload: { text: string; attachments: ComposerAttachment[]; profile?: string | null }
 ): null | QueuedPromptEntry => {
   const sid = sidOf(key)
 
@@ -92,6 +93,7 @@ export const enqueueQueuedPrompt = (
     id: nextId(),
     text: payload.text,
     attachments: cloneAttachments(payload.attachments),
+    ...(payload.profile?.trim() ? { profile: payload.profile.trim() } : {}),
     queuedAt: Date.now()
   }
 
diff --git a/apps/desktop/src/store/gateway.ts b/apps/desktop/src/store/gateway.ts
index 9b0f037b2ac6..062809354589 100644
--- a/apps/desktop/src/store/gateway.ts
+++ b/apps/desktop/src/store/gateway.ts
@@ -202,6 +202,23 @@ export async function openGatewayForProfile(profile: string): Promise<void> {
   }
 }
 
+// Resolve a profile's live gateway WITHOUT making it the foreground gateway.
+// Background queue drains use this so an offscreen profile can resume/submit
+// work without changing the active profile, composer state, or route.
+export async function ensureGatewayOpenForProfile(profile: string): Promise<HermesGateway | null> {
+  const key = normKey(profile)
+
+  if (key === primaryProfile) {
+    return isOpen(primaryGateway) ? primaryGateway : null
+  }
+
+  await openGatewayForProfile(key)
+
+  const gateway = secondaries.get(key)?.gateway ?? null
+
+  return isOpen(gateway) ? gateway : null
+}
+
 // Make `profile` the active gateway, lazily opening its socket if needed. The
 // primary is a no-op fast path. Background sockets are never closed here.
 export async function ensureGatewayForProfile(profile: string): Promise<void> {