diff --git a/assistant/src/__tests__/host-bash-proxy.test.ts b/assistant/src/__tests__/host-bash-proxy.test.ts
index fe9c4dc5246..834d001a0e5 100644
--- a/assistant/src/__tests__/host-bash-proxy.test.ts
+++ b/assistant/src/__tests__/host-bash-proxy.test.ts
@@ -16,14 +16,22 @@ mock.module("../config/loader.js", () => ({
 }));
 
 const sentMessages: unknown[] = [];
+const sentMessageOptions: unknown[] = [];
 const resolvedInteractionIds: string[] = [];
 let mockHasClient = false;
+let mockCapableClients: Array<{ clientId: string; capabilities: string[] }> = [];
+let mockClientRegistry: Map<string, { clientId: string; capabilities: string[] }> = new Map();
 
 mock.module("../runtime/assistant-event-hub.js", () => ({
-  broadcastMessage: (msg: unknown) => sentMessages.push(msg),
+  broadcastMessage: (msg: unknown, _conversationId?: string, options?: unknown) => {
+    sentMessages.push(msg);
+    sentMessageOptions.push(options);
+  },
   assistantEventHub: {
     getMostRecentClientByCapability: (cap: string) =>
       cap === "host_bash" && mockHasClient ? { id: "mock-client" } : null,
+    listClientsByCapability: (_cap: string) => mockCapableClients,
+    getClientById: (clientId: string) => mockClientRegistry.get(clientId),
   },
 }));
 
@@ -45,11 +53,30 @@ describe("HostBashProxy", () => {
 
   function setup() {
     sentMessages.length = 0;
+    sentMessageOptions.length = 0;
     resolvedInteractionIds.length = 0;
     mockHasClient = false;
+    mockCapableClients = [];
+    mockClientRegistry = new Map();
     proxy = new (HostBashProxy as any)();
   }
 
+  function setupSingleClient(clientId = "client-1") {
+    const entry = { clientId, capabilities: ["host_bash"] };
+    mockCapableClients = [entry];
+    mockClientRegistry.set(clientId, entry);
+  }
+
+  function setupMultipleClients(clientIds: string[]) {
+    mockCapableClients = clientIds.map((id) => ({
+      clientId: id,
+      capabilities: ["host_bash"],
+    }));
+    for (const entry of mockCapableClients) {
+      mockClientRegistry.set(entry.clientId, entry);
+    }
+  }
+
   afterEach(() => {
     proxy?.dispose();
     HostBashProxy.reset();
@@ -528,4 +555,184 @@ describe("HostBashProxy", () => {
       expect(resolvedInteractionIds).toEqual([]);
     });
   });
+
+  describe("target client routing", () => {
+    test("auto-resolves when exactly one capable client is connected", async () => {
+      setup();
+      setupSingleClient("client-abc");
+
+      const resultPromise = proxy.request(
+        { command: "echo hello" },
+        "session-1",
+      );
+
+      expect(sentMessages).toHaveLength(1);
+      const sent = sentMessages[0] as Record<string, unknown>;
+      expect(sent.targetClientId).toBe("client-abc");
+
+      // Options passed to broadcastMessage should also have targetClientId
+      const opts = sentMessageOptions[0] as Record<string, unknown> | undefined;
+      expect(opts?.targetClientId).toBe("client-abc");
+
+      const requestId = sent.requestId as string;
+      proxy.resolve(requestId, {
+        stdout: "hello\n",
+        stderr: "",
+        exitCode: 0,
+        timedOut: false,
+      });
+
+      const result = await resultPromise;
+      expect(result.isError).toBe(false);
+    });
+
+    test("uses explicit targetClientId when it is valid", async () => {
+      setup();
+      setupSingleClient("client-abc");
+      // Also register a second client so we're sure explicit targeting works
+      const entry2 = { clientId: "client-xyz", capabilities: ["host_bash"] };
+      mockCapableClients.push(entry2);
+      mockClientRegistry.set("client-xyz", entry2);
+
+      const resultPromise = proxy.request(
+        { command: "echo hello", targetClientId: "client-abc" },
+        "session-1",
+      );
+
+      expect(sentMessages).toHaveLength(1);
+      const sent = sentMessages[0] as Record<string, unknown>;
+      expect(sent.targetClientId).toBe("client-abc");
+
+      const opts = sentMessageOptions[0] as Record<string, unknown> | undefined;
+      expect(opts?.targetClientId).toBe("client-abc");
+
+      const requestId = sent.requestId as string;
+      proxy.resolve(requestId, {
+        stdout: "ok\n",
+        stderr: "",
+        exitCode: 0,
+        timedOut: false,
+      });
+
+      const result = await resultPromise;
+      expect(result.isError).toBe(false);
+    });
+
+    test("returns error for explicit targetClientId that is not connected", async () => {
+      setup();
+      setupSingleClient("client-abc");
+
+      const result = await proxy.request(
+        { command: "echo hello", targetClientId: "client-unknown" },
+        "session-1",
+      );
+
+      // Should return error without broadcasting
+      expect(result.isError).toBe(true);
+      expect(result.content).toContain("client-unknown");
+      expect(result.content).toContain("assistant clients list --capability host_bash");
+      expect(sentMessages).toHaveLength(0);
+    });
+
+    test("returns error for explicit targetClientId that is connected but lacks host_bash", async () => {
+      setup();
+      // Register a client without host_bash capability
+      mockClientRegistry.set("client-no-bash", {
+        clientId: "client-no-bash",
+        capabilities: [],
+      });
+
+      const result = await proxy.request(
+        { command: "echo hello", targetClientId: "client-no-bash" },
+        "session-1",
+      );
+
+      expect(result.isError).toBe(true);
+      expect(result.content).toContain("client-no-bash");
+      expect(result.content).toContain("does not support host_bash");
+      expect(sentMessages).toHaveLength(0);
+    });
+
+    test("falls through to untargeted broadcast when multiple capable clients are connected and no targetClientId", async () => {
+      setup();
+      setupMultipleClients(["client-1", "client-2", "client-3"]);
+
+      const resultPromise = proxy.request(
+        { command: "echo hello" },
+        "session-1",
+      );
+
+      // Should broadcast without an early error return
+      expect(sentMessages).toHaveLength(1);
+      const sent = sentMessages[0] as Record<string, unknown>;
+      expect(sent.type).toBe("host_bash_request");
+      // No target client resolved — untargeted broadcast
+      expect(sent.targetClientId).toBeUndefined();
+
+      const opts = sentMessageOptions[0] as Record<string, unknown> | undefined;
+      expect(opts?.targetClientId).toBeUndefined();
+
+      // Manually resolve to clean up
+      const requestId = sent.requestId as string;
+      proxy.resolve(requestId, {
+        stdout: "hello\n",
+        stderr: "",
+        exitCode: 0,
+        timedOut: false,
+      });
+
+      const result = await resultPromise;
+      expect(result.isError).toBe(false);
+    });
+
+    test("falls through to broadcast when zero capable clients (existing timeout path)", async () => {
+      setup();
+      // mockCapableClients is empty (default), so capableClients.length === 0
+
+      const resultPromise = proxy.request(
+        { command: "echo hello" },
+        "session-1",
+      );
+
+      // Should still broadcast (no early return)
+      expect(sentMessages).toHaveLength(1);
+      const sent = sentMessages[0] as Record<string, unknown>;
+      expect(sent.type).toBe("host_bash_request");
+      // targetClientId is undefined when no clients present
+      expect(sent.targetClientId).toBeUndefined();
+
+      // Manually resolve to clean up
+      const requestId = sent.requestId as string;
+      proxy.resolve(requestId, {
+        stdout: "",
+        stderr: "",
+        exitCode: 0,
+        timedOut: false,
+      });
+
+      await resultPromise;
+    });
+
+    test("includes targetClientId in timeout error message when client was resolved", async () => {
+      setup();
+      setupSingleClient("client-mac");
+
+      jest.useFakeTimers();
+      try {
+        const resultPromise = proxy.request(
+          { command: "echo slow", timeout_seconds: 30 },
+          "session-1",
+        );
+
+        // Proxy timeout = 33s; advance past it
+        jest.advanceTimersByTime(34 * 1000);
+
+        const result = await resultPromise;
+        expect(result.isError).toBe(true);
+        expect(result.content).toContain("client-mac");
+      } finally {
+        jest.useRealTimers();
+      }
+    });
+  });
 });
diff --git a/assistant/src/daemon/host-bash-proxy.ts b/assistant/src/daemon/host-bash-proxy.ts
index 1efa1ceb753..d08ca459c72 100644
--- a/assistant/src/daemon/host-bash-proxy.ts
+++ b/assistant/src/daemon/host-bash-proxy.ts
@@ -21,6 +21,7 @@ interface PendingRequest {
   conversationId: string;
   /** Detach the abort listener from the caller's signal. No-op when no signal was passed. */
   detachAbort: () => void;
+  targetClientId?: string;
 }
 
 export class HostBashProxy {
@@ -69,6 +70,7 @@ export class HostBashProxy {
       working_dir?: string;
       timeout_seconds?: number;
       env?: Record<string, string>;
+      targetClientId?: string;
     },
     conversationId: string,
     signal?: AbortSignal,
@@ -78,6 +80,28 @@ export class HostBashProxy {
       return Promise.resolve(result);
     }
 
+    const capableClients = assistantEventHub.listClientsByCapability("host_bash");
+
+    let resolvedTargetClientId: string | undefined;
+
+    if (input.targetClientId) {
+      const target = assistantEventHub.getClientById(input.targetClientId);
+      if (!target || !target.capabilities.includes("host_bash")) {
+        return Promise.resolve({
+          content: `Error: client "${input.targetClientId}" is not connected or does not support host_bash. Run \`assistant clients list --capability host_bash\` to see available clients.`,
+          isError: true,
+        });
+      }
+      resolvedTargetClientId = input.targetClientId;
+    } else if (capableClients.length === 1) {
+      // Auto-resolve when exactly one capable client is connected.
+      resolvedTargetClientId = capableClients[0].clientId;
+    }
+    // capableClients.length === 0 or > 1 without explicit target: resolvedTargetClientId
+    // stays undefined and falls through to untargeted broadcast — the existing timeout/error
+    // path handles the zero-client case, and multi-client ambiguity is enforced at the tool
+    // executor layer (not here) once target_client_id is exposed in the tool schema.
+
     const requestId = uuid();
 
     return new Promise<ToolExecutionResult>((resolve, reject) => {
@@ -98,10 +122,13 @@ export class HostBashProxy {
           { requestId, command: input.command },
           "Host bash proxy request timed out",
         );
+        const timeoutMessage = resolvedTargetClientId
+          ? `Host bash proxy timed out waiting for response from client ${resolvedTargetClientId}`
+          : "Host bash proxy timed out waiting for client response";
         resolve(
           formatShellOutput(
             "",
-            "Host bash proxy timed out waiting for client response",
+            timeoutMessage,
             null,
             true,
             timeoutSec,
@@ -139,20 +166,26 @@ export class HostBashProxy {
         timeoutSec,
         conversationId,
         detachAbort,
+        targetClientId: resolvedTargetClientId,
       });
 
       try {
-        broadcastMessage({
-          type: "host_bash_request",
-          requestId,
+        broadcastMessage(
+          {
+            type: "host_bash_request",
+            requestId,
+            conversationId,
+            command: input.command,
+            working_dir: input.working_dir,
+            timeout_seconds: input.timeout_seconds,
+            targetClientId: resolvedTargetClientId,
+            ...(input.env && Object.keys(input.env).length > 0
+                ? { env: input.env }
+                : {}),
+          },
           conversationId,
-          command: input.command,
-          working_dir: input.working_dir,
-          timeout_seconds: input.timeout_seconds,
-          ...(input.env && Object.keys(input.env).length > 0
-              ? { env: input.env }
-              : {}),
-          });
+          { targetClientId: resolvedTargetClientId },
+        );
       } catch (err) {
         clearTimeout(timer);
         this.pending.delete(requestId);