diff --git a/assistant/src/daemon/conversation-surfaces.ts b/assistant/src/daemon/conversation-surfaces.ts
index 6df0eaa781a..962e0990bba 100644
--- a/assistant/src/daemon/conversation-surfaces.ts
+++ b/assistant/src/daemon/conversation-surfaces.ts
@@ -1780,6 +1780,10 @@ export async function surfaceProxyResolver(
     // Record the action and proxy to the connected desktop client
     const reasoning =
       typeof input.reasoning === "string" ? input.reasoning : undefined;
+    const targetClientId =
+      typeof input.target_client_id === "string" && input.target_client_id !== ""
+        ? input.target_client_id
+        : undefined;
     ctx.hostCuProxy.recordAction(toolName, input, reasoning);
     return ctx.hostCuProxy.request(
       toolName,
@@ -1788,6 +1792,7 @@ export async function surfaceProxyResolver(
       ctx.hostCuProxy.stepCount,
       reasoning,
       signal,
+      targetClientId,
     );
   }
 
diff --git a/assistant/src/tools/computer-use/definitions.ts b/assistant/src/tools/computer-use/definitions.ts
index 0d237092761..7bbd9db4da0 100644
--- a/assistant/src/tools/computer-use/definitions.ts
+++ b/assistant/src/tools/computer-use/definitions.ts
@@ -63,6 +63,11 @@ export const computerUseClickTool: Tool = {
             description:
               "Explanation of what you see and why you are clicking here",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["reasoning"],
       },
@@ -99,6 +104,11 @@ export const computerUseTypeTextTool: Tool = {
             type: "string",
             description: "Explanation of what you are typing and why",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["text", "reasoning"],
       },
@@ -136,6 +146,11 @@ export const computerUseKeyTool: Tool = {
             type: "string",
             description: "Explanation of why you are pressing this key",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["key", "reasoning"],
       },
@@ -190,6 +205,11 @@ export const computerUseScrollTool: Tool = {
             type: "string",
             description: "Explanation of why you are scrolling",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["direction", "amount", "reasoning"],
       },
@@ -250,6 +270,11 @@ export const computerUseDragTool: Tool = {
             type: "string",
             description: "Explanation of what you are dragging and why",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["reasoning"],
       },
@@ -285,6 +310,11 @@ export const computerUseWaitTool: Tool = {
             type: "string",
             description: "Explanation of what you are waiting for",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["duration_ms", "reasoning"],
       },
@@ -323,6 +353,11 @@ export const computerUseOpenAppTool: Tool = {
             description:
               "Explanation of why you need to open or switch to this app",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["app_name", "reasoning"],
       },
@@ -360,6 +395,11 @@ export const computerUseRunAppleScriptTool: Tool = {
             description:
               "Explanation of what this script does and why AppleScript is better than UI interaction for this step",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to target. Required when multiple clients support host_cu; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_cu`.",
+          },
         },
         required: ["script", "reasoning"],
       },
diff --git a/assistant/src/tools/host-filesystem/edit.ts b/assistant/src/tools/host-filesystem/edit.ts
index 4100ff260e1..4c606d4eb3a 100644
--- a/assistant/src/tools/host-filesystem/edit.ts
+++ b/assistant/src/tools/host-filesystem/edit.ts
@@ -1,6 +1,8 @@
+import { supportsHostProxy } from "../../channels/types.js";
 import { HostFileProxy } from "../../daemon/host-file-proxy.js";
 import { RiskLevel } from "../../permissions/types.js";
 import type { ToolDefinition } from "../../providers/types.js";
+import { assistantEventHub } from "../../runtime/assistant-event-hub.js";
 import { FileSystemOps } from "../shared/filesystem/file-ops-service.js";
 import { formatEditDiff } from "../shared/filesystem/format-diff.js";
 import { hostPolicy } from "../shared/filesystem/path-policy.js";
@@ -37,6 +39,11 @@ class HostFileEditTool implements Tool {
             description:
               "Replace all occurrences instead of requiring a unique match (default: false)",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to execute this on. Required when multiple clients support host_file; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_file`.",
+          },
         },
         required: ["path", "old_string", "new_string"],
       },
@@ -84,6 +91,24 @@ class HostFileEditTool implements Tool {
 
     const replaceAll = input.replace_all === true;
 
+    const targetClientId =
+      typeof input.target_client_id === "string" && input.target_client_id !== ""
+        ? input.target_client_id
+        : undefined;
+
+    const transportInterface = context.transportInterface;
+    if (
+      targetClientId == null &&
+      transportInterface != null &&
+      !supportsHostProxy(transportInterface) &&
+      assistantEventHub.listClientsByCapability("host_file").length > 1
+    ) {
+      return {
+        content: `Error: multiple clients support host_file. Specify which client to use with \`target_client_id\`. Run \`assistant clients list --capability host_file\` to see client IDs and labels.`,
+        isError: true,
+      };
+    }
+
     // Proxy to connected client for execution on the user's machine
     // when a capable client is available (managed/cloud-hosted mode).
     if (HostFileProxy.instance.isAvailable()) {
@@ -94,6 +119,7 @@ class HostFileEditTool implements Tool {
           old_string: oldString as string,
           new_string: newString as string,
           replace_all: replaceAll,
+          targetClientId,
         },
         context.conversationId,
         context.signal,
diff --git a/assistant/src/tools/host-filesystem/read.ts b/assistant/src/tools/host-filesystem/read.ts
index a41220255a8..bfe219701d0 100644
--- a/assistant/src/tools/host-filesystem/read.ts
+++ b/assistant/src/tools/host-filesystem/read.ts
@@ -1,8 +1,10 @@
 import { extname } from "node:path";
 
+import { supportsHostProxy } from "../../channels/types.js";
 import { HostFileProxy } from "../../daemon/host-file-proxy.js";
 import { RiskLevel } from "../../permissions/types.js";
 import type { ToolDefinition } from "../../providers/types.js";
+import { assistantEventHub } from "../../runtime/assistant-event-hub.js";
 import { FileSystemOps } from "../shared/filesystem/file-ops-service.js";
 import {
   IMAGE_EXTENSIONS,
@@ -37,6 +39,11 @@ class HostFileReadTool implements Tool {
             type: "number",
             description: "Maximum number of lines to read",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to execute this on. Required when multiple clients support host_file; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_file`.",
+          },
         },
         required: ["path"],
       },
@@ -55,6 +62,24 @@ class HostFileReadTool implements Tool {
       };
     }
 
+    const targetClientId =
+      typeof input.target_client_id === "string" && input.target_client_id !== ""
+        ? input.target_client_id
+        : undefined;
+
+    const transportInterface = context.transportInterface;
+    if (
+      targetClientId == null &&
+      transportInterface != null &&
+      !supportsHostProxy(transportInterface) &&
+      assistantEventHub.listClientsByCapability("host_file").length > 1
+    ) {
+      return {
+        content: `Error: multiple clients support host_file. Specify which client to use with \`target_client_id\`. Run \`assistant clients list --capability host_file\` to see client IDs and labels.`,
+        isError: true,
+      };
+    }
+
     // Proxy to connected client for execution on the user's machine
     // when a capable client is available (managed/cloud-hosted mode),
     // including image reads that need the host filesystem view.
@@ -65,6 +90,7 @@ class HostFileReadTool implements Tool {
           path: rawPath,
           offset: typeof input.offset === "number" ? input.offset : undefined,
           limit: typeof input.limit === "number" ? input.limit : undefined,
+          targetClientId,
         },
         context.conversationId,
         context.signal,
diff --git a/assistant/src/tools/host-filesystem/write.ts b/assistant/src/tools/host-filesystem/write.ts
index 3113545ef61..be23354bd7c 100644
--- a/assistant/src/tools/host-filesystem/write.ts
+++ b/assistant/src/tools/host-filesystem/write.ts
@@ -1,6 +1,8 @@
+import { supportsHostProxy } from "../../channels/types.js";
 import { HostFileProxy } from "../../daemon/host-file-proxy.js";
 import { RiskLevel } from "../../permissions/types.js";
 import type { ToolDefinition } from "../../providers/types.js";
+import { assistantEventHub } from "../../runtime/assistant-event-hub.js";
 import { FileSystemOps } from "../shared/filesystem/file-ops-service.js";
 import { formatWriteSummary } from "../shared/filesystem/format-diff.js";
 import { hostPolicy } from "../shared/filesystem/path-policy.js";
@@ -28,6 +30,11 @@ class HostFileWriteTool implements Tool {
             type: "string",
             description: "The content to write to the file",
           },
+          target_client_id: {
+            type: "string",
+            description:
+              "ID of the specific client to execute this on. Required when multiple clients support host_file; omit when only one is connected. Obtain IDs from `assistant clients list --capability host_file`.",
+          },
         },
         required: ["path", "content"],
       },
@@ -54,6 +61,24 @@ class HostFileWriteTool implements Tool {
       };
     }
 
+    const targetClientId =
+      typeof input.target_client_id === "string" && input.target_client_id !== ""
+        ? input.target_client_id
+        : undefined;
+
+    const transportInterface = context.transportInterface;
+    if (
+      targetClientId == null &&
+      transportInterface != null &&
+      !supportsHostProxy(transportInterface) &&
+      assistantEventHub.listClientsByCapability("host_file").length > 1
+    ) {
+      return {
+        content: `Error: multiple clients support host_file. Specify which client to use with \`target_client_id\`. Run \`assistant clients list --capability host_file\` to see client IDs and labels.`,
+        isError: true,
+      };
+    }
+
     // Proxy to connected client for execution on the user's machine
     // when a capable client is available (managed/cloud-hosted mode).
     if (HostFileProxy.instance.isAvailable()) {
@@ -62,6 +87,7 @@ class HostFileWriteTool implements Tool {
           operation: "write",
           path: rawPath,
           content: fileContent,
+          targetClientId,
         },
         context.conversationId,
         context.signal,