diff --git a/desktop/src/features/agents/lib/pickProfileAgent.test.mjs b/desktop/src/features/agents/lib/pickProfileAgent.test.mjs
index 710b5fc4be8..e404b8c4dd5 100644
--- a/desktop/src/features/agents/lib/pickProfileAgent.test.mjs
+++ b/desktop/src/features/agents/lib/pickProfileAgent.test.mjs
@@ -33,6 +33,24 @@ test("the shared profile target prefers the active persona instance", () => {
   assert.equal(pickProfileAgent([running, stopped], NONE_ARCHIVED), running);
 });
 
+test("the active community identity wins over a running sibling", () => {
+  const legacy = agent({
+    pubkey: "a".repeat(64),
+    relayUrl: "wss://legacy.example",
+    status: "running",
+  });
+  const current = agent({
+    pubkey: "b".repeat(64),
+    relayUrl: "wss://current.example",
+    status: "stopped",
+  });
+
+  assert.equal(
+    pickProfileAgent([legacy, current], NONE_ARCHIVED, "wss://current.example"),
+    current,
+  );
+});
+
 test("an archived instance early in file order cannot hijack the target", () => {
   const archived = agent({
     name: "Archived instance",
diff --git a/desktop/src/features/agents/lib/pickProfileAgent.ts b/desktop/src/features/agents/lib/pickProfileAgent.ts
index dc2437c86ea..6e795a01bcc 100644
--- a/desktop/src/features/agents/lib/pickProfileAgent.ts
+++ b/desktop/src/features/agents/lib/pickProfileAgent.ts
@@ -12,15 +12,22 @@ import type { ManagedAgent } from "@/shared/api/types";
  * file order can't hijack the persona target. Returns `undefined` when every
  * instance is archived — the card then renders in persona-only mode. The
  * `isArchived` predicate is fail-open (returns `false` while the relay archive
- * snapshot loads), so a cold start never briefly picks nothing.
+ * snapshot loads), so a cold start never briefly picks nothing. When the same
+ * persona has identities from several communities, the active community's
+ * identity wins before runtime status.
  */
 export function pickProfileAgent(
   agents: readonly ManagedAgent[],
   isArchived: (pubkey: string) => boolean,
+  preferredRelayUrl?: string,
 ) {
   return [...agents]
     .filter((agent) => !isArchived(agent.pubkey))
     .sort((left, right) => {
+      const relayDiff =
+        Number(right.relayUrl === preferredRelayUrl) -
+        Number(left.relayUrl === preferredRelayUrl);
+      if (relayDiff !== 0) return relayDiff;
       const activeDiff =
         Number(isManagedAgentActive(right)) -
         Number(isManagedAgentActive(left));
diff --git a/desktop/src/features/agents/ui/UnifiedAgentsSection.tsx b/desktop/src/features/agents/ui/UnifiedAgentsSection.tsx
index d0ff2e2738a..42349a3f684 100644
--- a/desktop/src/features/agents/ui/UnifiedAgentsSection.tsx
+++ b/desktop/src/features/agents/ui/UnifiedAgentsSection.tsx
@@ -9,6 +9,7 @@ import { resolveAgentCardModelLabel } from "@/features/agents/lib/agentCardModel
 import { friendlyAgentLastError } from "@/features/agents/lib/friendlyAgentLastError";
 import { isManagedAgentActive } from "@/features/agents/lib/managedAgentControlActions";
 import { pickProfileAgent } from "@/features/agents/lib/pickProfileAgent";
+import { useCommunities } from "@/features/communities/useCommunities";
 import { useIsArchivedPredicate } from "@/features/identity-archive/hooks";
 import { useUserProfileQuery } from "@/features/profile/hooks";
 import type { AgentPersona, ManagedAgent } from "@/shared/api/types";
@@ -95,6 +96,7 @@ export function UnifiedAgentsSection(props: UnifiedAgentsSectionProps) {
     onDeletePersona,
   } = props;
 
+  const { activeCommunity } = useCommunities();
   const isArchived = useIsArchivedPredicate();
   const { groups, ungrouped, unknown } = React.useMemo(
     () => buildUnifiedGroups(personas, agents, isArchived),
@@ -131,7 +133,11 @@ export function UnifiedAgentsSection(props: UnifiedAgentsSectionProps) {
               onClick={onOpenCatalog}
             />
             {groups.map((group) => {
-              const profileAgent = pickProfileAgent(group.agents, isArchived);
+              const profileAgent = pickProfileAgent(
+                group.agents,
+                isArchived,
+                activeCommunity?.relayUrl,
+              );
               return (
                 <AgentPersonaCard
                   actions={(effectiveAvatarUrl, isEffectiveAvatarLoading) => (
diff --git a/desktop/src/features/agents/ui/UnifiedAgentsSectionCardTarget.test.mjs b/desktop/src/features/agents/ui/UnifiedAgentsSectionCardTarget.test.mjs
index 690a921040e..e94aab0655b 100644
--- a/desktop/src/features/agents/ui/UnifiedAgentsSectionCardTarget.test.mjs
+++ b/desktop/src/features/agents/ui/UnifiedAgentsSectionCardTarget.test.mjs
@@ -40,6 +40,7 @@ let screen;
 let createElement;
 let QueryClient;
 let QueryClientProvider;
+let CommunitiesProvider;
 let UnifiedAgentsSection;
 
 const ipcHandlers = new Map();
@@ -118,7 +119,11 @@ function renderSection(props) {
     createElement(
       QueryClientProvider,
       { client },
-      createElement(UnifiedAgentsSection, props),
+      createElement(
+        CommunitiesProvider,
+        null,
+        createElement(UnifiedAgentsSection, props),
+      ),
     ),
   );
 }
@@ -127,6 +132,7 @@ before(async () => {
   Object.assign(globalThis, {
     document: dom.window.document,
     HTMLElement: dom.window.HTMLElement,
+    localStorage: dom.window.localStorage,
     window: dom.window,
     IS_REACT_ACT_ENVIRONMENT: true,
   });
@@ -156,6 +162,9 @@ before(async () => {
   ({ QueryClient, QueryClientProvider } = await import(
     "@tanstack/react-query"
   ));
+  ({ CommunitiesProvider } = await import(
+    "@/features/communities/useCommunities"
+  ));
   ({ UnifiedAgentsSection } = await import("./UnifiedAgentsSection.tsx"));
 });
 
diff --git a/desktop/src/features/agents/ui/useManagedAgentActions.ts b/desktop/src/features/agents/ui/useManagedAgentActions.ts
index 0627ad6ac36..caf35204d7c 100644
--- a/desktop/src/features/agents/ui/useManagedAgentActions.ts
+++ b/desktop/src/features/agents/ui/useManagedAgentActions.ts
@@ -17,6 +17,7 @@ import {
 import { useGlobalAgentConfig } from "@/features/agents/useGlobalAgentConfig";
 import { useChannelsQuery } from "@/features/channels/hooks";
 import { invalidateChannelMembersRosters } from "@/features/channels/rosterFreshness";
+import { useCommunities } from "@/features/communities/useCommunities";
 import { usePresenceQuery } from "@/features/presence/hooks";
 import type { AgentPersona, Channel, ManagedAgent } from "@/shared/api/types";
 import { removeChannelMember } from "@/shared/api/tauri";
@@ -38,6 +39,7 @@ import {
 export function useManagedAgentActions() {
   const queryClient = useQueryClient();
   const { globalConfig } = useGlobalAgentConfig();
+  const { activeCommunity } = useCommunities();
   const relayAgentsQuery = useRelayAgentsQuery();
   const managedAgentsQuery = useManagedAgentsQuery();
   const [shouldLoadChannels, setShouldLoadChannels] = React.useState(false);
@@ -166,7 +168,12 @@ export function useManagedAgentActions() {
       if (!agent) return;
       await startManagedAgentWithRules({
         agent,
-        startManagedAgent: startMutation.mutateAsync,
+        startManagedAgent: (agentPubkey) =>
+          startMutation.mutateAsync({
+            pubkey: agentPubkey,
+            expectedRelayUrl: activeCommunity?.relayUrl,
+            expectedSignerPubkey: activeCommunity?.pubkey,
+          }),
       });
     } catch (error) {
       setActionErrorMessage(
@@ -186,7 +193,12 @@ export function useManagedAgentActions() {
       if (!agent) return;
       await respawnManagedAgentWithRules({
         agent,
-        startManagedAgent: startMutation.mutateAsync,
+        startManagedAgent: (agentPubkey) =>
+          startMutation.mutateAsync({
+            pubkey: agentPubkey,
+            expectedRelayUrl: activeCommunity?.relayUrl,
+            expectedSignerPubkey: activeCommunity?.pubkey,
+          }),
         stopManagedAgent: stopMutation.mutateAsync,
         onStopped: () => clearActiveTurnsForAgentOnStop(agent.pubkey),
       });