diff --git a/apps/server/src/device/DeviceHubOperations.ts b/apps/server/src/device/DeviceHubOperations.ts
index 9371484f4c93f..131e3b95241ae 100644
--- a/apps/server/src/device/DeviceHubOperations.ts
+++ b/apps/server/src/device/DeviceHubOperations.ts
@@ -7,7 +7,7 @@ import {
 import * as Duration from "effect/Duration";
 import * as Effect from "effect/Effect";
 import * as Schema from "effect/Schema";
-import { HttpClient, HttpClientRequest, HttpClientResponse } from "effect/http";
+import { HttpClient, HttpClientError, HttpClientRequest, HttpClientResponse } from "effect/http";
 
 import type { DeviceHostReady, DeviceOperations, HostDevice } from "./DeviceHost.ts";
 
@@ -239,7 +239,10 @@ export const makeDeviceHubOperations = (options: {
           (cause) =>
             new DeviceOperationError({
               operation: "screenshot",
-              reason: "request_failed",
+              reason:
+                HttpClientError.isHttpClientError(cause) && cause.reason._tag === "StatusCodeError"
+                  ? "hub_rejected"
+                  : "request_failed",
               cause,
             }),
         ),
diff --git a/apps/server/src/device/DeviceService.test.ts b/apps/server/src/device/DeviceService.test.ts
index a9ff957b91997..b97a7f2a320d4 100644
--- a/apps/server/src/device/DeviceService.test.ts
+++ b/apps/server/src/device/DeviceService.test.ts
@@ -42,6 +42,37 @@ const decodeJson = Schema.decodeUnknownSync(Schema.fromJsonString(Schema.Unknown
 const decodeBootError = Schema.decodeUnknownSync(Schema.fromJsonString(DeviceBootError));
 const encodeBootError = Schema.encodeSync(Schema.fromJsonString(DeviceBootError));
 
+it.effect.each([400, 500])(
+  "distinguishes screenshot HTTP rejection (%s) from transport failure",
+  (status) =>
+    Effect.gen(function* () {
+      const operations = makeDeviceHubOperations({
+        hostId: LOCAL_DEVICE_HOST_ID,
+        origin: "http://device.test",
+        http: HttpClient.make((request) =>
+          Effect.succeed(
+            HttpClientResponse.fromWeb(request, new Response("private hub output", { status })),
+          ),
+        ),
+        run: () => Effect.die("Screenshot does not run a command"),
+        androidAvailable: Effect.succeed(false),
+      });
+      const result = yield* operations
+        .screenshot({
+          id: "phone",
+          name: "Phone",
+          version: "iOS 26.3",
+          platform: "ios",
+          booted: true,
+          physical: false,
+        })
+        .pipe(Effect.result);
+      expect(result).toMatchObject({
+        failure: { _tag: "DeviceOperationError", reason: "hub_rejected" },
+      });
+    }),
+);
+
 const fixture = Effect.fn("fixture")(function* (
   onBoot: Effect.Effect<void> = Effect.void,
   bootError?: string | { error?: string; errors?: Array<{ message: string; error?: string }> },
diff --git a/apps/server/src/mcp/McpHttpServer.test.ts b/apps/server/src/mcp/McpHttpServer.test.ts
index 1f77dbfcc087d..902785778a975 100644
--- a/apps/server/src/mcp/McpHttpServer.test.ts
+++ b/apps/server/src/mcp/McpHttpServer.test.ts
@@ -5,6 +5,8 @@ import { expect, it } from "@effect/vitest";
 import { NodeHttpServer } from "@effect/platform-node";
 import * as NodeServices from "@effect/platform-node/NodeServices";
 import {
+  DeviceId,
+  DeviceOperationError,
   EnvironmentId,
   OrchestratorMcpEnvironmentTarget,
   OrchestratorMcpFailure,
@@ -24,6 +26,7 @@ import { McpSchema, McpServer, Tool, Toolkit } from "effect/ai";
 import { HttpBody, HttpClient, HttpClientRequest, HttpRouter } from "effect/http";
 
 import * as ProjectService from "../project/ProjectService.ts";
+import * as DeviceService from "../device/DeviceService.ts";
 import * as PullRequestReviewGuideService from "../pullRequest/PullRequestReviewGuideService.ts";
 import * as ServerConfig from "../config.ts";
 import * as ServerSettings from "../serverSettings.ts";
@@ -140,6 +143,86 @@ const callTool = (name: string, args: Record<string, unknown>) =>
 
 const callSnapshot = (args: Record<string, unknown>) => callTool("preview_snapshot", args);
 
+it.effect.each([
+  { input: {}, open: false, message: "No device is open in this thread. Call device_open first." },
+  {
+    input: { deviceId: "missing", hostId: "local" },
+    open: false,
+    message: "Device missing is not open in this thread. Call device_open first.",
+  },
+  {
+    input: {},
+    open: true,
+    message:
+      "Device screenshot failed: Could not communicate with device support. Try refreshing devices.",
+  },
+  {
+    input: {},
+    open: true,
+    rejected: true,
+    message:
+      "Device screenshot failed: The device hub could not complete the request. Call device_list to check the device state, and device_open if it needs to be reopened.",
+  },
+])(
+  "preserves actionable screenshot failure text: $message",
+  ({ input, open, message, ...options }) =>
+    Effect.gen(function* () {
+      const server = yield* McpServer.McpServer;
+      const result = yield* server.callTool({ name: "device_screenshot", arguments: input }).pipe(
+        Effect.provideService(McpInvocationContext.McpInvocationContext, {
+          ...invocation,
+          capabilities: new Set(["device"] as const),
+        }),
+        Effect.provideService(McpSchema.McpServerClient, client),
+      );
+      expect(result.isError).toBe(true);
+      expect(result.content).toEqual([{ type: "text", text: message }]);
+      expect(result.structuredContent).toMatchObject({
+        error: { message, operation: "screenshot" },
+      });
+      expect(JSON.stringify(result)).not.toContain("private hub output");
+    }).pipe(
+      Effect.provide(
+        McpHttpServer.layerDeviceToolkit.pipe(
+          Layer.provideMerge(McpServer.McpServer.layer),
+          Layer.provide(McpToolAccessTestkit.liveThreadsLayer),
+          Layer.provide(
+            Layer.mock(DeviceService.DeviceService)({
+              locateSession: () => Effect.succeedNone,
+              sessionsForThread: () =>
+                Effect.succeed(
+                  open
+                    ? [
+                        {
+                          threadId,
+                          hostId: "local",
+                          deviceId: DeviceId.make("phone"),
+                          platform: "ios",
+                          openedAt: "2026-10-23T00:00:00Z",
+                        },
+                      ]
+                    : [],
+                ),
+              screenshot: () =>
+                Effect.fail(
+                  new DeviceOperationError({
+                    operation: "screenshot",
+                    reason:
+                      "rejected" in options && options.rejected ? "hub_rejected" : "request_failed",
+                    cause: new Error("private hub output"),
+                  }),
+                ),
+            }),
+          ),
+          Layer.provide(Layer.mock(ProjectService.ProjectService)({})),
+          Layer.provide(ServerConfig.layerTest(process.cwd(), { prefix: "t3-device-mcp-test-" })),
+          Layer.provide(NodeServices.layer),
+        ),
+      ),
+      Effect.scoped,
+    ),
+);
+
 const layerRecordingTools = (calls: Array<unknown>) => {
   const RecordingToolkit = Toolkit.make(
     OrchestratorToolkit.tools.delegate_task,
diff --git a/apps/server/src/mcp/McpHttpServer.ts b/apps/server/src/mcp/McpHttpServer.ts
index 4365267e2144d..e684316f48d9a 100644
--- a/apps/server/src/mcp/McpHttpServer.ts
+++ b/apps/server/src/mcp/McpHttpServer.ts
@@ -766,10 +766,14 @@ const registerDeviceScreenshot = Effect.fn("McpHttpServer.registerDeviceScreensh
         Effect.provideService(ThreadManagementService.ThreadManagementService, threads),
       ),
     "screenshot",
-    (error) =>
-      isDeviceToolError(error) || isOrchestratorMcpFailure(error)
-        ? error.message
-        : "Device screenshot failed.",
+    (error) => {
+      if (!isDeviceToolError(error)) {
+        return isOrchestratorMcpFailure(error) ? error.message : "Device screenshot failed.";
+      }
+      return error._tag === "DeviceOperationError" && error.reason === "hub_rejected"
+        ? `${error.message} Call device_list to check the device state, and device_open if it needs to be reopened.`
+        : error.message;
+    },
   );
 });