diff --git a/assistant/openapi.yaml b/assistant/openapi.yaml
index 7412c80eb73..44dbf3aad74 100644
--- a/assistant/openapi.yaml
+++ b/assistant/openapi.yaml
@@ -5893,6 +5893,10 @@ paths:
                 required:
                   - accepted
                 additionalProperties: false
+        "400":
+          description: x-vellum-client-id header is missing for a targeted host bash request.
+        "403":
+          description: Submitting client does not match the targeted client for this request.
       requestBody:
         required: true
         content:
diff --git a/assistant/src/__tests__/host-bash-routes.test.ts b/assistant/src/__tests__/host-bash-routes.test.ts
new file mode 100644
index 00000000000..4927876443e
--- /dev/null
+++ b/assistant/src/__tests__/host-bash-routes.test.ts
@@ -0,0 +1,291 @@
+/**
+ * Unit tests for the /v1/host-bash-result route handler.
+ *
+ * Covers the client-identity validation introduced by the targeted-host-proxy
+ * plan: when a pending interaction has a `targetClientId`, the submitting
+ * client must supply a matching `x-vellum-client-id` header or be rejected
+ * with 400 (missing) or 403 (mismatch).
+ */
+import { afterAll, beforeEach, describe, expect, mock, test } from "bun:test";
+
+// ── Module mocks ─────────────────────────────────────────────────────
+
+mock.module("../config/env.js", () => ({
+  isHttpAuthDisabled: () => true,
+  hasUngatedHttpAuthDisabled: () => false,
+}));
+
+import type { PendingInteraction } from "../runtime/pending-interactions.js";
+
+// Stored pending interactions keyed by requestId.
+const pendingStore = new Map<string, PendingInteraction>();
+const resolvedIds: string[] = [];
+
+mock.module("../runtime/pending-interactions.js", () => ({
+  get: (requestId: string) => pendingStore.get(requestId),
+  resolve: (requestId: string) => {
+    const entry = pendingStore.get(requestId);
+    if (entry) {
+      pendingStore.delete(requestId);
+      resolvedIds.push(requestId);
+    }
+    return entry;
+  },
+}));
+
+interface ResolveCall {
+  requestId: string;
+  result: { stdout: string; stderr: string; exitCode: number | null; timedOut: boolean };
+}
+
+const resolveSpy: ResolveCall[] = [];
+
+mock.module("../daemon/host-bash-proxy.js", () => ({
+  HostBashProxy: {
+    get instance() {
+      return {
+        resolve(
+          requestId: string,
+          result: { stdout: string; stderr: string; exitCode: number | null; timedOut: boolean },
+        ) {
+          resolveSpy.push({ requestId, result });
+        },
+      };
+    },
+  },
+}));
+
+// ── Real imports (after mocks) ───────────────────────────────────────
+
+import {
+  BadRequestError,
+  ConflictError,
+  ForbiddenError,
+  NotFoundError,
+} from "../runtime/routes/errors.js";
+import { ROUTES } from "../runtime/routes/host-bash-routes.js";
+
+afterAll(() => {
+  mock.restore();
+});
+
+const handleHostBashResult = ROUTES.find(
+  (r) => r.endpoint === "host-bash-result",
+)!.handler;
+
+// ── Helpers ──────────────────────────────────────────────────────────
+
+function registerPending(
+  requestId: string,
+  overrides: Partial<PendingInteraction> = {},
+): void {
+  pendingStore.set(requestId, {
+    conversationId: "conv-1",
+    kind: "host_bash",
+    ...overrides,
+  });
+}
+
+function bashBody(requestId: string): Record<string, unknown> {
+  return {
+    requestId,
+    stdout: "hello\n",
+    stderr: "",
+    exitCode: 0,
+    timedOut: false,
+  };
+}
+
+// ── Tests ────────────────────────────────────────────────────────────
+
+describe("handleHostBashResult", () => {
+  beforeEach(() => {
+    pendingStore.clear();
+    resolvedIds.length = 0;
+    resolveSpy.length = 0;
+  });
+
+  // ── Happy paths ────────────────────────────────────────────────────
+
+  describe("untargeted request (no targetClientId)", () => {
+    test("accepts when header is present", async () => {
+      const requestId = "req-untargeted-with-header";
+      registerPending(requestId);
+
+      const result = await handleHostBashResult({
+        body: bashBody(requestId),
+        headers: { "x-vellum-client-id": "client-abc" },
+      });
+
+      expect(result).toEqual({ accepted: true });
+      expect(resolveSpy).toHaveLength(1);
+      expect(resolvedIds).toContain(requestId);
+    });
+
+    test("accepts when header is absent", async () => {
+      const requestId = "req-untargeted-no-header";
+      registerPending(requestId);
+
+      const result = await handleHostBashResult({
+        body: bashBody(requestId),
+      });
+
+      expect(result).toEqual({ accepted: true });
+      expect(resolveSpy).toHaveLength(1);
+      expect(resolvedIds).toContain(requestId);
+    });
+  });
+
+  describe("targeted request (targetClientId set)", () => {
+    test("accepts when x-vellum-client-id matches targetClientId", async () => {
+      const requestId = "req-targeted-match";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      const result = await handleHostBashResult({
+        body: bashBody(requestId),
+        headers: { "x-vellum-client-id": "client-abc" },
+      });
+
+      expect(result).toEqual({ accepted: true });
+      expect(resolveSpy).toHaveLength(1);
+      expect(resolveSpy[0].requestId).toBe(requestId);
+      expect(resolvedIds).toContain(requestId);
+    });
+
+    test("trims whitespace from x-vellum-client-id before comparing", async () => {
+      const requestId = "req-targeted-trim";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      const result = await handleHostBashResult({
+        body: bashBody(requestId),
+        headers: { "x-vellum-client-id": "  client-abc  " },
+      });
+
+      expect(result).toEqual({ accepted: true });
+    });
+  });
+
+  // ── Error: missing header on targeted request ──────────────────────
+
+  describe("targeted request — missing x-vellum-client-id header", () => {
+    test("throws BadRequestError (400) when header is absent", () => {
+      const requestId = "req-targeted-no-header";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      expect(() =>
+        handleHostBashResult({ body: bashBody(requestId) }),
+      ).toThrow(BadRequestError);
+    });
+
+    test("throws BadRequestError (400) when header is empty string", () => {
+      const requestId = "req-targeted-empty-header";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      expect(() =>
+        handleHostBashResult({
+          body: bashBody(requestId),
+          headers: { "x-vellum-client-id": "   " },
+        }),
+      ).toThrow(BadRequestError);
+    });
+
+    test("interaction is NOT resolved on 400 (still pending)", () => {
+      const requestId = "req-targeted-no-header-stays";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      try {
+        handleHostBashResult({ body: bashBody(requestId) });
+      } catch {
+        // expected
+      }
+
+      expect(resolvedIds).not.toContain(requestId);
+      expect(pendingStore.has(requestId)).toBe(true);
+    });
+  });
+
+  // ── Error: wrong client ────────────────────────────────────────────
+
+  describe("targeted request — mismatched x-vellum-client-id", () => {
+    test("throws ForbiddenError (403) when client ID does not match", () => {
+      const requestId = "req-targeted-mismatch";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      expect(() =>
+        handleHostBashResult({
+          body: bashBody(requestId),
+          headers: { "x-vellum-client-id": "client-xyz" },
+        }),
+      ).toThrow(ForbiddenError);
+    });
+
+    test("ForbiddenError message names both the submitting and expected client", () => {
+      const requestId = "req-targeted-mismatch-msg";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      let caught: unknown;
+      try {
+        handleHostBashResult({
+          body: bashBody(requestId),
+          headers: { "x-vellum-client-id": "client-xyz" },
+        });
+      } catch (e) {
+        caught = e;
+      }
+
+      expect(caught).toBeInstanceOf(ForbiddenError);
+      const msg = (caught as ForbiddenError).message;
+      expect(msg).toContain("client-xyz");
+      expect(msg).toContain("client-abc");
+    });
+
+    test("interaction is NOT resolved on 403 (still pending)", () => {
+      const requestId = "req-targeted-mismatch-stays";
+      registerPending(requestId, { targetClientId: "client-abc" });
+
+      try {
+        handleHostBashResult({
+          body: bashBody(requestId),
+          headers: { "x-vellum-client-id": "client-xyz" },
+        });
+      } catch {
+        // expected
+      }
+
+      expect(resolvedIds).not.toContain(requestId);
+      expect(pendingStore.has(requestId)).toBe(true);
+    });
+  });
+
+  // ── Other existing validations (regression) ────────────────────────
+
+  test("throws BadRequestError when body is missing", () => {
+    expect(() => handleHostBashResult({})).toThrow(BadRequestError);
+  });
+
+  test("throws BadRequestError when requestId is missing", () => {
+    expect(() =>
+      handleHostBashResult({ body: { stdout: "x" } }),
+    ).toThrow(BadRequestError);
+  });
+
+  test("throws NotFoundError for unknown requestId", () => {
+    expect(() =>
+      handleHostBashResult({
+        body: bashBody("unknown-req-id"),
+      }),
+    ).toThrow(NotFoundError);
+  });
+
+  test("throws ConflictError when pending interaction is not host_bash kind", () => {
+    const requestId = "req-wrong-kind";
+    pendingStore.set(requestId, {
+      conversationId: "conv-1",
+      kind: "confirmation",
+    });
+
+    expect(() =>
+      handleHostBashResult({ body: bashBody(requestId) }),
+    ).toThrow(ConflictError);
+  });
+});
diff --git a/assistant/src/runtime/routes/host-bash-routes.ts b/assistant/src/runtime/routes/host-bash-routes.ts
index 19a4fd48a41..f1eab46844b 100644
--- a/assistant/src/runtime/routes/host-bash-routes.ts
+++ b/assistant/src/runtime/routes/host-bash-routes.ts
@@ -11,6 +11,7 @@ import * as pendingInteractions from "../pending-interactions.js";
 import {
   BadRequestError,
   ConflictError,
+  ForbiddenError,
   NotFoundError,
 } from "./errors.js";
 import type { RouteDefinition, RouteHandlerArgs } from "./types.js";
@@ -19,7 +20,7 @@ import type { RouteDefinition, RouteHandlerArgs } from "./types.js";
 // POST /v1/host-bash-result
 // ---------------------------------------------------------------------------
 
-function handleHostBashResult({ body }: RouteHandlerArgs) {
+function handleHostBashResult({ body, headers }: RouteHandlerArgs) {
   if (!body || typeof body !== "object") {
     throw new BadRequestError("Request body is required");
   }
@@ -36,6 +37,8 @@ function handleHostBashResult({ body }: RouteHandlerArgs) {
     throw new BadRequestError("requestId is required");
   }
 
+  const submittingClientId = headers?.["x-vellum-client-id"]?.trim() || undefined;
+
   const peeked = pendingInteractions.get(requestId);
   if (!peeked) {
     throw new NotFoundError(
@@ -49,6 +52,20 @@ function handleHostBashResult({ body }: RouteHandlerArgs) {
     );
   }
 
+  const { targetClientId } = peeked;
+  if (targetClientId) {
+    if (!submittingClientId) {
+      throw new BadRequestError(
+        "x-vellum-client-id header is required for targeted host bash requests",
+      );
+    }
+    if (submittingClientId !== targetClientId) {
+      throw new ForbiddenError(
+        `Client "${submittingClientId}" is not the target for this request (expected "${targetClientId}"). The targeted client must submit the result.`,
+      );
+    }
+  }
+
   pendingInteractions.resolve(requestId);
 
   HostBashProxy.instance.resolve(requestId, {
@@ -84,6 +101,16 @@ export const ROUTES: RouteDefinition[] = [
     responseBody: z.object({
       accepted: z.boolean(),
     }),
+    additionalResponses: {
+      "400": {
+        description:
+          "x-vellum-client-id header is missing for a targeted host bash request.",
+      },
+      "403": {
+        description:
+          "Submitting client does not match the targeted client for this request.",
+      },
+    },
     handler: handleHostBashResult,
   },
 ];
diff --git a/clients/shared/Network/GatewayHTTPClient.swift b/clients/shared/Network/GatewayHTTPClient.swift
index a0ac9503128..7cd4dfa9337 100644
--- a/clients/shared/Network/GatewayHTTPClient.swift
+++ b/clients/shared/Network/GatewayHTTPClient.swift
@@ -106,15 +106,22 @@ public enum GatewayHTTPClient {
     ///   - body: Optional HTTP body data.
     ///   - params: Optional query parameters. Keys and values are percent-encoded
     ///     using a restricted character set that escapes `&`, `=`, `+`, and `#`.
+    ///   - contentType: Optional Content-Type override. Defaults to `application/json`.
+    ///   - extraHeaders: Optional additional headers to include in the request.
     ///   - timeout: Request timeout in seconds. Defaults to 30.
     /// - Returns: A `Response` with the raw data and HTTP status code.
     /// - Throws: `ClientError` if the request cannot be constructed, or network errors from `URLSession`.
-    public static func post(path: String, body: Data? = nil, params: [String: String]? = nil, contentType: String? = nil, timeout: TimeInterval = 30, unprefixed: Bool = false) async throws -> Response {
+    public static func post(path: String, body: Data? = nil, params: [String: String]? = nil, contentType: String? = nil, extraHeaders: [String: String]? = nil, timeout: TimeInterval = 30, unprefixed: Bool = false) async throws -> Response {
         return try await executeWithRetry(path: path, params: params, method: "POST", timeout: timeout, unprefixed: unprefixed) { request in
             request.httpBody = body
             if let contentType {
                 request.setValue(contentType, forHTTPHeaderField: "Content-Type")
             }
+            if let extraHeaders {
+                for (k, v) in extraHeaders {
+                    request.setValue(v, forHTTPHeaderField: k)
+                }
+            }
         }
     }
 
diff --git a/clients/shared/Network/HostProxyClient.swift b/clients/shared/Network/HostProxyClient.swift
index 1593324cd2f..9348e94510a 100644
--- a/clients/shared/Network/HostProxyClient.swift
+++ b/clients/shared/Network/HostProxyClient.swift
@@ -24,6 +24,7 @@ public struct HostProxyClient: HostProxyClientProtocol {
             let response = try await GatewayHTTPClient.post(
                 path: "host-bash-result",
                 body: body,
+                extraHeaders: ["X-Vellum-Client-Id": DeviceIdStore.getOrCreate()],
                 timeout: 30
             )
             guard response.isSuccess else {