diff --git a/apps/desktop/src/app/contrib/session-rpc-dispatcher.test.ts b/apps/desktop/src/app/contrib/session-rpc-dispatcher.test.ts
index cee4203f44..2a5517e3bc 100644
--- a/apps/desktop/src/app/contrib/session-rpc-dispatcher.test.ts
+++ b/apps/desktop/src/app/contrib/session-rpc-dispatcher.test.ts
@@ -44,7 +44,7 @@ const { _resetSessionOwnerHintsForTests, setCronSessions, setMessagingSessions,
   await import('@/store/session')
 
 const { isSessionOwnerResolutionError } = await import('@/store/session-owner-resolution')
-const { $sessionTiles } = await import('@/store/session-states')
+const { $sessionTiles, recordSessionEventScope } = await import('@/store/session-states')
 const { makeSessionInfo } = await import('@/test/session-info')
 
 function dispatcher(
@@ -208,6 +208,88 @@ describe('createSessionRpcDispatcher: exact owner rungs', () => {
   })
 })
 
+describe('createSessionRpcDispatcher: routes by the session OWNING connection when two connections share a profile name', () => {
+  // Two registered connections, both exposing `default` (the default install:
+  // this device + a remote gateway), and the window's primary is the OTHER
+  // connection. A bare profile name carries no connection identity, and the
+  // profile door (requestGatewayForProfile -> gatewayForProfile) resolves a
+  // bare name equal to the primary profile against the PRIMARY socket — a
+  // different machine than the one holding the session. The inbound event
+  // already proved which socket owns the runtime, so that exact owner has to
+  // outrank the connection-blind row profile: otherwise the 2nd prompt of a
+  // `This device` chat is answered by the remote backend with
+  // `4001 session not found`.
+  function twoConnections(): void {
+    $connectionsRegistry.set({ connections: [{ id: 'local' }, { id: 'homelab' }] } as never)
+  }
+
+  it('routes a session that lives on the LOCAL connection back to that connection', async () => {
+    gatewayMocks.activeConnectionId = 'homelab'
+    twoConnections()
+    recordSessionEventScope({ connectionId: 'local', profile: 'default', session_id: 'rt-local' })
+    setSessions([makeSessionInfo({ id: 'rt-local', profile: 'default' })])
+    const { ambientRequest, request } = dispatcher()
+
+    await expect(request('prompt.submit', { session_id: 'rt-local', text: 'again' })).resolves.toEqual({
+      routed: true
+    })
+
+    expect(gatewayMocks.requestGatewayForAgent).toHaveBeenCalledWith('local', 'default', 'prompt.submit', {
+      session_id: 'rt-local',
+      text: 'again'
+    })
+    expect(gatewayMocks.requestGatewayForProfile).not.toHaveBeenCalled()
+    expect(ambientRequest).not.toHaveBeenCalled()
+  })
+
+  it('routes a session that lives on the REMOTE connection to that connection', async () => {
+    gatewayMocks.activeConnectionId = 'local'
+    twoConnections()
+    recordSessionEventScope({ connectionId: 'homelab', profile: 'default', session_id: 'rt-remote' })
+    setSessions([makeSessionInfo({ id: 'rt-remote', profile: 'default' })])
+    const { ambientRequest, request } = dispatcher()
+
+    await expect(request('prompt.submit', { session_id: 'rt-remote', text: 'again' })).resolves.toEqual({
+      routed: true
+    })
+
+    expect(gatewayMocks.requestGatewayForAgent).toHaveBeenCalledWith('homelab', 'default', 'prompt.submit', {
+      session_id: 'rt-remote',
+      text: 'again'
+    })
+    expect(gatewayMocks.requestGatewayForProfile).not.toHaveBeenCalled()
+    expect(ambientRequest).not.toHaveBeenCalled()
+  })
+
+  it('keeps a connection-tagged row owner over a conflicting event scope', async () => {
+    gatewayMocks.activeConnectionId = 'homelab'
+    twoConnections()
+    setSessions([makeSessionInfo({ connection_id: 'source-b', id: 'stored-shared', profile: 'default' })])
+    recordSessionEventScope({ connectionId: 'local', profile: 'default', session_id: 'stored-shared' })
+
+    await expect(dispatcher().request('session.resume', { session_id: 'stored-shared' })).resolves.toEqual({
+      routed: true
+    })
+
+    expect(gatewayMocks.requestGatewayForAgent).toHaveBeenLastCalledWith('source-b', 'default', 'session.resume', {
+      session_id: 'stored-shared'
+    })
+  })
+
+  it('leaves a request with NO session context on the ambient socket, ledger or not', async () => {
+    gatewayMocks.activeConnectionId = 'homelab'
+    twoConnections()
+    recordSessionEventScope({ connectionId: 'local', profile: 'default', session_id: 'rt-local' })
+    const { ambientRequest, request } = dispatcher()
+
+    await expect(request('config.get', {})).resolves.toEqual({ ambient: true })
+
+    expect(ambientRequest).toHaveBeenCalledWith('config.get', {})
+    expect(gatewayMocks.requestGatewayForAgent).not.toHaveBeenCalled()
+    expect(gatewayMocks.requestGatewayForProfile).not.toHaveBeenCalled()
+  })
+})
+
 describe('createSessionRpcDispatcher: stale runtime recovery', () => {
   it('requests a durable rebind for the visible session after a structured 4001', async () => {
     setSessions([makeSessionInfo({ connection_id: 'local', id: 'stored-omar', profile: 'omar' })])
diff --git a/apps/desktop/src/app/contrib/session-rpc-dispatcher.ts b/apps/desktop/src/app/contrib/session-rpc-dispatcher.ts
index d57bcbb115..b9f61b2445 100644
--- a/apps/desktop/src/app/contrib/session-rpc-dispatcher.ts
+++ b/apps/desktop/src/app/contrib/session-rpc-dispatcher.ts
@@ -39,7 +39,12 @@ import { isSessionGoneForBackgroundPolling } from '@/store/runtime-gone'
 import { getSessionOwnerHint, knownSessionOwner, ownerLookupSessionRows, requestSessionResume } from '@/store/session'
 import { assertSessionOwnerResolved } from '@/store/session-owner-resolution'
 import { requestForSessionProfile, type SessionOwnerScope } from '@/store/session-request-router'
-import { $focusedStoredSessionId, sessionTileOwnerRoute, storedSessionIdForRuntimeId } from '@/store/session-states'
+import {
+  $focusedStoredSessionId,
+  runtimeSessionOwner,
+  sessionTileOwnerRoute,
+  storedSessionIdForRuntimeId
+} from '@/store/session-states'
 
 import { findStoredIdForRuntimeId, resolveRoutingSessionId, resolveSessionRpcOwner } from './wiring-routing'
 
@@ -75,6 +80,14 @@ export function createSessionRpcDispatcher(deps: SessionRpcDispatcherDeps): Ambi
     })
 
     let owner: SessionOwnerScope = resolveSessionRpcOwner({
+      // An owner an inbound runtime event already proved for THIS session (#97511):
+      // the exact (connectionId, profile) of the socket that delivered its
+      // events. It outranks the connection-blind row/rung profile — the rung
+      // that makes two connections sharing a profile name collapse onto the
+      // primary socket (another machine) instead of the session's own.
+      eventOwner: storedSessionId =>
+        runtimeSessionOwner(storedSessionId) ??
+        (paramSessionId && paramSessionId !== storedSessionId ? runtimeSessionOwner(paramSessionId) : undefined),
       routingSessionId,
       sessionOwnerHint: storedSessionId => getSessionOwnerHint(storedSessionId),
       sessionRowOwner: storedSessionId => knownSessionOwner(ownerLookupSessionRows(), storedSessionId),
diff --git a/apps/desktop/src/app/contrib/wiring-routing.ts b/apps/desktop/src/app/contrib/wiring-routing.ts
index 0c6fef02a5..c0d8835b8a 100644
--- a/apps/desktop/src/app/contrib/wiring-routing.ts
+++ b/apps/desktop/src/app/contrib/wiring-routing.ts
@@ -5,7 +5,7 @@
  * React/Electron controller module.
  */
 
-import type { SessionOwnerRoute } from '@/store/session-request-router'
+import type { SessionOwnerRoute, SessionOwnerScope } from '@/store/session-request-router'
 
 import { SETTINGS_ROUTE } from '../routes'
 
@@ -61,6 +61,11 @@ export function resolveRoutingSessionId(args: {
  *  "active"). The type-only import keeps this module runtime-import-free. */
 export type SessionRpcOwnerRoute = SessionOwnerRoute
 
+/** A connection-bearing owner. Checked structurally so this module stays
+ *  runtime-import-free (the type guard lives in store/session-request-router). */
+const isRouteOwner = (owner: unknown): owner is SessionRpcOwnerRoute =>
+  Boolean(owner && typeof owner === 'object' && 'connectionId' in owner)
+
 /**
  * The SYNC owner a session-scoped RPC routes to, resolved in this order:
  *
@@ -73,9 +78,21 @@ export type SessionRpcOwnerRoute = SessionOwnerRoute
  *      list splice, or a tag carried across a refresh), else its bare
  *      profile (the cross-profile aggregator tags rows, but a bare profile
  *      loses the connection and can lag the create);
- *   4. undefined → the caller runs the cross-profile probe, and fails closed
+ *   4. `eventOwner`, an exact route an inbound runtime event already proved
+ *      for this session (store/session-states sessionOwnerByRuntimeId). It is
+ *      consulted whenever every rung above named nothing better than a bare
+ *      profile name, because a bare profile has NO connection: the profile
+ *      door (requestGatewayForProfile → gatewayForProfile) resolves a bare
+ *      name equal to the primary profile against the PRIMARY socket, so an
+ *      ordinary session that runs on a non-primary connection — two
+ *      connections both exposing `default` is enough — has its RPCs answered
+ *      by another machine ("4001 session not found" from the 2nd prompt on);
+ *   5. undefined → the caller runs the cross-profile probe, and fails closed
  *      if that misses too.
  *
+ * An EXACT durable route (1–3 tagged, or 4) always outranks a bare profile
+ * name; only a genuinely unknown owner falls through.
+ *
  * The hint outranks the row because the row is presentation state that can
  * be stamped from the AMBIENT profile (an optimistic row minted while
  * All-profiles / Bot routing left `default` active), and because it carries
@@ -90,18 +107,22 @@ export function resolveSessionRpcOwner(args: {
   tileOwnerRoute: (storedSessionId: string) => SessionRpcOwnerRoute | undefined
   sessionOwnerHint: (storedSessionId: string) => SessionRpcOwnerRoute | undefined
   sessionRowOwner: (storedSessionId: string) => null | SessionRpcOwnerRoute | string | undefined
+  eventOwner?: (storedSessionId: string) => SessionOwnerScope | undefined
 }): SessionRpcOwnerRoute | string | undefined {
-  const { routingSessionId, sessionOwnerHint, sessionRowOwner, tileOwnerRoute } = args
+  const { eventOwner, routingSessionId, sessionOwnerHint, sessionRowOwner, tileOwnerRoute } = args
 
   if (!routingSessionId) {
     return undefined
   }
 
   const fromRow = sessionRowOwner(routingSessionId)
+  const rowOwner = typeof fromRow === 'string' ? fromRow.trim() || undefined : (fromRow ?? undefined)
 
-  return (
-    tileOwnerRoute(routingSessionId) ??
-    sessionOwnerHint(routingSessionId) ??
-    (typeof fromRow === 'string' ? fromRow.trim() || undefined : (fromRow ?? undefined))
-  )
+  const durable = tileOwnerRoute(routingSessionId) ?? sessionOwnerHint(routingSessionId) ?? rowOwner
+
+  if (isRouteOwner(durable)) {
+    return durable
+  }
+
+  return eventOwner?.(routingSessionId) ?? durable
 }
diff --git a/apps/desktop/src/app/session/hooks/use-session-actions/utils.ts b/apps/desktop/src/app/session/hooks/use-session-actions/utils.ts
index 47119752c7..7ae23f45d8 100644
--- a/apps/desktop/src/app/session/hooks/use-session-actions/utils.ts
+++ b/apps/desktop/src/app/session/hooks/use-session-actions/utils.ts
@@ -39,7 +39,7 @@ import {
   setYoloActive
 } from '@/store/session'
 import type { SessionProfileRoute } from '@/store/session-request-router'
-import { sessionTileOwnerRoute } from '@/store/session-states'
+import { runtimeSessionOwner, sessionTileOwnerRoute } from '@/store/session-states'
 
 // Re-exported for the many session-actions/tile call sites that already import
 // it from here; the canonical definition lives in @/store/session.
@@ -1625,7 +1625,8 @@ export async function resolveSessionOwner(storedSessionId: null | string): Promi
     routingSessionId: storedSessionId,
     tileOwnerRoute: sessionTileOwnerRoute,
     sessionOwnerHint: getSessionOwnerHint,
-    sessionRowOwner: id => knownSessionOwner(ownerLookupSessionRows(), id)
+    sessionRowOwner: id => knownSessionOwner(ownerLookupSessionRows(), id),
+    eventOwner: runtimeSessionOwner
   })
 
   if (owner) {
diff --git a/apps/desktop/src/store/session-states.test.ts b/apps/desktop/src/store/session-states.test.ts
index 522cd2c1c1..2d522bf810 100644
--- a/apps/desktop/src/store/session-states.test.ts
+++ b/apps/desktop/src/store/session-states.test.ts
@@ -1301,6 +1301,25 @@ describe('knownOwnerForSession / requestForOwnedSession (#91684 client half)', (
     expect(knownOwnerForSession('stored-shared')).toEqual({ connectionId: 'source-b', profile: 'default' })
   })
 
+  // Two connections both exposing `default`: the row only names the profile,
+  // and a bare profile is resolved by the profile door against the PRIMARY
+  // connection — another machine for a session that runs on a non-primary one.
+  // The inbound event proved the exact owner, so it must outrank the
+  // connection-blind row profile (this is what keeps the 2nd prompt of an
+  // ordinary session from answering `4001 session not found`).
+  it('prefers an event-proven connection over a bare row profile when two connections share the profile name', () => {
+    recordSessionEventScope({ connectionId: 'local', profile: 'default', session_id: 'rt-local' })
+    setSessions([{ id: 'rt-local', profile: 'default' } as never])
+
+    expect(knownOwnerForSession('rt-local')).toEqual({ connectionId: 'local', profile: 'default' })
+  })
+
+  it('still answers with the bare row profile when no event ever named the connection', () => {
+    setSessions([{ id: 'rt-unproven', profile: 'default' } as never])
+
+    expect(knownOwnerForSession('rt-unproven')).toBe('default')
+  })
+
   it('returns undefined (ambient) when no owner is known, and for null ids', () => {
     expect(knownOwnerForSession('unknown-session')).toBeUndefined()
     expect(knownOwnerForSession(null)).toBeUndefined()
diff --git a/apps/desktop/src/store/session-states.ts b/apps/desktop/src/store/session-states.ts
index b663c9e6fa..5c6ff6e9fd 100644
--- a/apps/desktop/src/store/session-states.ts
+++ b/apps/desktop/src/store/session-states.ts
@@ -59,6 +59,7 @@ import { secondaryProfileOwnerForEvent } from './session-event-provenance'
 import { $focusedTreePaneId } from './session-focus'
 import { assertSessionOwnerResolved } from './session-owner-resolution'
 import {
+  isSessionOwnerRoute,
   requestForSessionProfile,
   type SessionOwnerRoute,
   type SessionOwnerScope,
@@ -118,6 +119,17 @@ export function recordSessionEventScope(event: { connectionId?: string; profile?
   }
 }
 
+/** The owner an inbound runtime EVENT proved for `sessionId` (#97511): the
+ *  exact (connectionId, profile) of the socket that delivered its events, or
+ *  the bare profile of a legacy profile-only pool. Exported so the session-scoped
+ *  RPC ladder can consult it WITHOUT the connection-blind profile rung
+ *  preempting it (see knownOwnerForSession). */
+export function runtimeSessionOwner(sessionId: null | string | undefined): SessionOwnerScope {
+  const id = String(sessionId ?? '').trim()
+
+  return id ? sessionOwnerByRuntimeId.get(id) : undefined
+}
+
 /** Forget only profile-pool runtime owners during permanent LOCAL profile
  * teardown. These string routes came exclusively from the legacy secondary
  * producer; exact connection descriptors must survive a same-named remote
@@ -1038,10 +1050,15 @@ export function openTileGatewayScopes(): Set<string> {
  * Last rung: the owner recorded from the inbound runtime event itself
  * (sessionOwnerByRuntimeId, #97511) — an orphan runtime whose tile/hint/row
  * binding is absent or stale still routes through the exact
- * (connectionId, profile) or secondary socket's proven local profile. Every
- * durable rung above keeps outranking it, so a stored-id collision never
- * inherits a stale runtime ledger entry. Unproven profile fields record
- * nothing, so unknown owners in multi-profile topology still fail closed.
+ * (connectionId, profile) or secondary socket's proven local profile. It sits
+ * BELOW every durable EXACT route, so a stored-id collision never inherits a
+ * stale runtime ledger entry, but it must sit ABOVE a bare profile name: a
+ * bare profile carries no connection, and the profile door resolves it against
+ * the PRIMARY connection (store/gateway gatewayForProfile), which for an
+ * ordinary session that runs on a non-primary connection — two connections
+ * both exposing `default` is enough — is another machine that answers
+ * `4001 session not found`. Unproven profile fields record nothing, so unknown
+ * owners in multi-profile topology still fail closed.
  * Returns undefined when no owner is known — the caller fails closed
  * (assertSessionOwnerResolved), never falls to "active".
  */
@@ -1052,12 +1069,16 @@ export function knownOwnerForSession(sessionId: null | string | undefined): Sess
 
   const storedSessionId = storedSessionIdForRuntimeId(sessionId) ?? sessionId
 
-  return (
+  const durable =
     sessionTileOwner(storedSessionId) ??
     getSessionOwnerHint(storedSessionId) ??
-    knownSessionOwner(ownerLookupSessionRows(), storedSessionId) ??
-    sessionOwnerByRuntimeId.get(sessionId)
-  )
+    knownSessionOwner(ownerLookupSessionRows(), storedSessionId)
+
+  if (isSessionOwnerRoute(durable)) {
+    return durable
+  }
+
+  return sessionOwnerByRuntimeId.get(sessionId) ?? durable
 }
 
 /**