diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/ChatInputFooter.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/ChatInputFooter.tsx
index 14ec71c7380..1cceca08b2e 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/ChatInputFooter.tsx
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/ChatInputFooter.tsx
@@ -49,6 +49,7 @@ interface ChatInputFooterProps {
 	pendingQuestion?: {
 		questionId: string;
 		question: string;
+		description?: string;
 		options?: { label: string; description?: string }[];
 	} | null;
 	isQuestionSubmitting?: boolean;
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/components/QuestionInputOverlay/QuestionInputOverlay.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/components/QuestionInputOverlay/QuestionInputOverlay.tsx
index 9064246551b..4af96469d6b 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/components/QuestionInputOverlay/QuestionInputOverlay.tsx
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ChatInputFooter/components/QuestionInputOverlay/QuestionInputOverlay.tsx
@@ -9,6 +9,7 @@ interface QuestionInputOverlayProps {
 	question: {
 		questionId: string;
 		question: string;
+		description?: string;
 		options?: QuestionOption[];
 	};
 	isSubmitting: boolean;
@@ -63,9 +64,16 @@ export function QuestionInputOverlay({
 		<div className="flex max-h-[300px] flex-col overflow-hidden rounded-[13px] border-[0.5px] border-border bg-foreground/[0.02]">
 			{/* Question — pinned header */}
 			<div className="flex shrink-0 items-start gap-2 px-3 pt-3 pb-3">
-				<p className="flex-1 text-sm leading-snug text-foreground">
-					{question.question}
-				</p>
+				<div className="flex-1 space-y-1">
+					<p className="text-sm leading-snug text-foreground">
+						{question.question}
+					</p>
+					{question.description && (
+						<p className="text-xs leading-snug text-muted-foreground">
+							{question.description}
+						</p>
+					)}
+				</div>
 				<Tooltip>
 					<TooltipTrigger asChild>
 						<button
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/ToolCallBlock.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/ToolCallBlock.tsx
index 1e3d3357a83..ab7498ccbe6 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/ToolCallBlock.tsx
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/ToolCallBlock.tsx
@@ -36,6 +36,7 @@ import { ListTaskStatusesToolCall } from "./components/ListTaskStatusesToolCall"
 import { ListTasksToolCall } from "./components/ListTasksToolCall";
 import { ListWorkspacesToolCall } from "./components/ListWorkspacesToolCall";
 import { LspInspectToolCall } from "./components/LspInspectToolCall";
+import { RequestSandboxAccessToolCall } from "./components/RequestSandboxAccessToolCall";
 import { SkillToolCall } from "./components/SkillToolCall";
 import { StartAgentSessionToolCall } from "./components/StartAgentSessionToolCall";
 import { SubagentToolCall } from "./components/SubagentToolCall";
@@ -614,8 +615,15 @@ export function ToolCallBlock({
 		);
 	}
 
-	if (toolName === "request_sandbox_access") {
-		return <SupersetToolCall part={part} toolName="Request sandbox access" />;
+	if (toolName === "request_access") {
+		return (
+			<RequestSandboxAccessToolCall
+				part={part}
+				args={args}
+				result={result}
+				isInterrupted={isInterrupted}
+			/>
+		);
 	}
 
 	if (toolName === "lsp_inspect") {
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/AskUserQuestionToolCall/AskUserQuestionToolCall.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/AskUserQuestionToolCall/AskUserQuestionToolCall.tsx
index 5fb7b93c428..245a903bcdd 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/AskUserQuestionToolCall/AskUserQuestionToolCall.tsx
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/AskUserQuestionToolCall/AskUserQuestionToolCall.tsx
@@ -8,6 +8,7 @@ import {
 } from "lucide-react";
 import { useMemo } from "react";
 import type { ToolPart } from "../../../../utils/tool-helpers";
+import { ToolStatusBadge } from "../ToolStatusBadge";
 
 interface QuestionToolOption {
 	label: string;
@@ -124,27 +125,6 @@ function findAnswerForQuestion({
 	return undefined;
 }
 
-type QuestionStatus = "awaiting" | "answered" | "cancelled";
-
-const QUESTION_STATUS_CONFIG: Record<
-	QuestionStatus,
-	{ label: string; icon: typeof ClockIcon }
-> = {
-	awaiting: { label: "Awaiting Response", icon: ClockIcon },
-	answered: { label: "Answered", icon: CheckIcon },
-	cancelled: { label: "Cancelled", icon: XIcon },
-};
-
-function QuestionStatusDescription({ status }: { status: QuestionStatus }) {
-	const { label, icon: Icon } = QUESTION_STATUS_CONFIG[status];
-	return (
-		<span className="ml-2 flex items-center gap-1 font-medium uppercase tracking-wide">
-			<Icon className="h-3 w-3 shrink-0" />
-			{label}
-		</span>
-	);
-}
-
 function toSingleQuestion(
 	args: Record<string, unknown>,
 ): QuestionToolQuestion[] {
@@ -267,11 +247,11 @@ export function AskUserQuestionToolCall({
 			title="Question"
 			description={
 				isPending ? (
-					<QuestionStatusDescription status="awaiting" />
+					<ToolStatusBadge icon={ClockIcon} label="Awaiting Response" />
 				) : isAnswered ? (
-					<QuestionStatusDescription status="answered" />
+					<ToolStatusBadge icon={CheckIcon} label="Answered" />
 				) : isCancelled || isCancelledByError || isCancelledByStop ? (
-					<QuestionStatusDescription status="cancelled" />
+					<ToolStatusBadge icon={XIcon} label="Cancelled" />
 				) : undefined
 			}
 		>
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/RequestSandboxAccessToolCall.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/RequestSandboxAccessToolCall.tsx
new file mode 100644
index 00000000000..f583d6a874f
--- /dev/null
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/RequestSandboxAccessToolCall.tsx
@@ -0,0 +1,123 @@
+import { ToolCallRow } from "@superset/ui/ai-elements/tool-call-row";
+import {
+	CheckIcon,
+	CircleXIcon,
+	ClockIcon,
+	FolderLockIcon,
+	XIcon,
+} from "lucide-react";
+import type { ComponentType } from "react";
+import type { ToolPart } from "../../../../utils/tool-helpers";
+import type { ToolStatusBadgeVariant } from "../ToolStatusBadge";
+import { ToolStatusBadge } from "../ToolStatusBadge";
+
+interface RequestSandboxAccessToolCallProps {
+	part: ToolPart;
+	args: Record<string, unknown>;
+	result: Record<string, unknown>;
+	isInterrupted?: boolean;
+}
+
+type AccessStatus = "pending" | "granted" | "denied" | "cancelled" | "error";
+
+const ACCESS_STATUS_CONFIG: Record<
+	AccessStatus,
+	{
+		icon: ComponentType<{ className?: string }>;
+		label: string;
+		variant?: ToolStatusBadgeVariant;
+	}
+> = {
+	pending: { icon: ClockIcon, label: "Awaiting Response" },
+	granted: { icon: CheckIcon, label: "Access Granted" },
+	denied: { icon: XIcon, label: "Access Denied" },
+	cancelled: { icon: XIcon, label: "Cancelled" },
+	error: { icon: CircleXIcon, label: "Error", variant: "danger" },
+};
+
+function toAccessDecision(content: string): "granted" | "denied" | null {
+	if (content.startsWith("Access already granted")) return "granted";
+	if (content.startsWith("Access granted")) return "granted";
+	if (content.startsWith("Access denied")) return "denied";
+	return null;
+}
+
+function toAccessStatus(
+	part: ToolPart,
+	result: Record<string, unknown>,
+	isInterrupted: boolean,
+): AccessStatus {
+	if (
+		isInterrupted &&
+		part.state !== "output-available" &&
+		part.state !== "output-error"
+	) {
+		return "cancelled";
+	}
+	if (part.state !== "output-available" && part.state !== "output-error") {
+		return "pending";
+	}
+	if (part.state === "output-error" || result.isError === true) {
+		return "error";
+	}
+	const content =
+		(typeof result.content === "string" && result.content.trim()) ||
+		(typeof result.text === "string" && result.text.trim()) ||
+		"";
+	return toAccessDecision(content) ?? "error";
+}
+
+export function RequestSandboxAccessToolCall({
+	part,
+	args,
+	result,
+	isInterrupted = false,
+}: RequestSandboxAccessToolCallProps) {
+	const requestedPath = typeof args.path === "string" ? args.path.trim() : null;
+	const reason = typeof args.reason === "string" ? args.reason.trim() : null;
+
+	const status = toAccessStatus(part, result, isInterrupted);
+	const { icon, label, variant } = ACCESS_STATUS_CONFIG[status];
+	const statusBadge = (
+		<ToolStatusBadge icon={icon} label={label} variant={variant} />
+	);
+
+	const isPending = status === "pending";
+	const isCancelledOrError = status === "cancelled" || status === "error";
+	const hasContext = Boolean(requestedPath || reason);
+
+	return (
+		<ToolCallRow
+			icon={FolderLockIcon}
+			isPending={false}
+			isError={false}
+			title="Request Access"
+			description={statusBadge}
+		>
+			{!isPending && hasContext ? (
+				<div className="space-y-1 px-3 py-2">
+					{requestedPath ? (
+						<div className="text-xs text-muted-foreground">
+							Path: {requestedPath}
+						</div>
+					) : null}
+					{reason ? (
+						<div className="text-xs text-muted-foreground">
+							Reason: {reason}
+						</div>
+					) : null}
+					{!isCancelledOrError ? (
+						<div className="text-sm text-foreground">
+							{status === "granted" ? "Access granted" : "Access denied"}
+						</div>
+					) : (
+						<div className="flex items-center gap-1 text-sm text-destructive">
+							<CircleXIcon className="h-3 w-3 shrink-0" />
+							Aborted
+						</div>
+					)}
+				</div>
+			) : undefined}
+		</ToolCallRow>
+	);
+}
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/index.ts b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/index.ts
new file mode 100644
index 00000000000..be4eeb9f3d8
--- /dev/null
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/RequestSandboxAccessToolCall/index.ts
@@ -0,0 +1 @@
+export { RequestSandboxAccessToolCall } from "./RequestSandboxAccessToolCall";
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/ToolStatusBadge.tsx b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/ToolStatusBadge.tsx
new file mode 100644
index 00000000000..c9368456f15
--- /dev/null
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/ToolStatusBadge.tsx
@@ -0,0 +1,34 @@
+import { cn } from "@superset/ui/lib/utils";
+import type { ComponentType } from "react";
+
+const VARIANT_CLASSES = {
+	default: "",
+	success: "text-emerald-500",
+	danger: "text-destructive",
+} as const;
+
+export type ToolStatusBadgeVariant = keyof typeof VARIANT_CLASSES;
+
+interface ToolStatusBadgeProps {
+	icon: ComponentType<{ className?: string }>;
+	label: string;
+	variant?: ToolStatusBadgeVariant;
+}
+
+export function ToolStatusBadge({
+	icon: Icon,
+	label,
+	variant = "default",
+}: ToolStatusBadgeProps) {
+	return (
+		<span
+			className={cn(
+				"ml-2 flex items-center gap-1 font-medium uppercase tracking-wide",
+				VARIANT_CLASSES[variant],
+			)}
+		>
+			<Icon className="h-3 w-3 shrink-0" />
+			{label}
+		</span>
+	);
+}
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/index.ts b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/index.ts
new file mode 100644
index 00000000000..0a5773c27ea
--- /dev/null
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/components/ToolCallBlock/components/ToolStatusBadge/index.ts
@@ -0,0 +1,2 @@
+export type { ToolStatusBadgeVariant } from "./ToolStatusBadge";
+export { ToolStatusBadge } from "./ToolStatusBadge";
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.test.ts b/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.test.ts
index 502c3d31a31..dcc55d947e4 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.test.ts
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.test.ts
@@ -17,9 +17,7 @@ describe("normalizeToolName", () => {
 		expect(normalizeToolName("web_extract")).toBe("web_fetch");
 		expect(normalizeToolName("ask_user")).toBe("ask_user_question");
 		expect(normalizeToolName("ast_smart_edit")).toBe("ast_smart_edit");
-		expect(normalizeToolName("request_sandbox_access")).toBe(
-			"request_sandbox_access",
-		);
+		expect(normalizeToolName("request_sandbox_access")).toBe("request_access");
 		expect(normalizeToolName("task_write")).toBe("task_write");
 		expect(normalizeToolName("task_check")).toBe("task_check");
 		expect(normalizeToolName("submit_plan")).toBe("submit_plan");
diff --git a/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.ts b/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.ts
index 2248a598674..6d493864ab6 100644
--- a/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.ts
+++ b/apps/desktop/src/renderer/components/Chat/ChatInterface/utils/tool-helpers.ts
@@ -29,7 +29,8 @@ const TOOL_NAME_ALIASES: Record<string, string> = {
 
 	// Keep explicit passthroughs for newer Mastra tool names
 	ast_smart_edit: "ast_smart_edit",
-	request_sandbox_access: "request_sandbox_access",
+	request_access: "request_access",
+	request_sandbox_access: "request_access",
 	task_write: "task_write",
 	task_check: "task_check",
 	submit_plan: "submit_plan",
diff --git a/packages/chat/src/server/trpc/service.test.ts b/packages/chat/src/server/trpc/service.test.ts
index 7adf7272d1e..af4f55e508b 100644
--- a/packages/chat/src/server/trpc/service.test.ts
+++ b/packages/chat/src/server/trpc/service.test.ts
@@ -20,14 +20,17 @@ mock.module("mastracode", () => ({
 
 const { ChatRuntimeService } = await import("./service");
 
-function createRuntime(): RuntimeSession {
+function createRuntime(options?: {
+	respondToQuestion?: RuntimeSession["harness"]["respondToQuestion"];
+}): RuntimeSession {
 	return {
 		sessionId: SESSION_ID,
 		cwd: CWD,
 		harness: {
 			abort: mock(() => {}),
 			respondToToolApproval: mock(async (payload: unknown) => payload),
-			respondToQuestion: mock(async (payload: unknown) => payload),
+			respondToQuestion:
+				options?.respondToQuestion ?? mock(async (payload: unknown) => payload),
 			respondToPlanApproval: mock(async (payload: unknown) => payload),
 		} as unknown as RuntimeSession["harness"],
 		mcpManager: null as RuntimeSession["mcpManager"],
@@ -39,11 +42,13 @@ function createRuntime(): RuntimeSession {
 			path: "/tmp/secret",
 			reason: "Need access",
 		},
+		answeredQuestionIds: new Set(),
+		pendingQuestionResponses: new Map(),
 	};
 }
 
-function createServiceHarness() {
-	const runtime = createRuntime();
+function createServiceHarness(options?: Parameters<typeof createRuntime>[0]) {
+	const runtime = createRuntime(options);
 	const service = new ChatRuntimeService({
 		headers: async () => ({}),
 		apiUrl: "http://localhost:3000",
@@ -134,4 +139,61 @@ describe("ChatRuntimeService control mutations", () => {
 		});
 		expect(runtime.pendingSandboxQuestion).toBeNull();
 	});
+
+	it("does not clear pending question state when question response fails", async () => {
+		const respondToQuestion = mock(async () => {
+			throw new Error("failed to answer");
+		}) as RuntimeSession["harness"]["respondToQuestion"];
+		const { caller, runtime } = createServiceHarness({ respondToQuestion });
+
+		await expect(
+			caller.session.question.respond({
+				sessionId: SESSION_ID,
+				cwd: CWD,
+				payload: { questionId: "sandbox-1", answer: "Yes" },
+			}),
+		).rejects.toThrow("failed to answer");
+
+		expect(runtime.answeredQuestionIds.has("sandbox-1")).toBe(false);
+		expect(runtime.pendingSandboxQuestion).toEqual({
+			questionId: "sandbox-1",
+			path: "/tmp/secret",
+			reason: "Need access",
+		});
+	});
+
+	it("deduplicates concurrent responses for the same question", async () => {
+		let resolveResponse: (value: unknown) => void = () => {};
+		const respondToQuestion = mock(
+			() =>
+				new Promise((resolve) => {
+					resolveResponse = resolve;
+				}),
+		) as RuntimeSession["harness"]["respondToQuestion"];
+		const { caller, runtime } = createServiceHarness({ respondToQuestion });
+		const payload = { questionId: "sandbox-1", answer: "Yes" };
+
+		const firstResponse = caller.session.question.respond({
+			sessionId: SESSION_ID,
+			cwd: CWD,
+			payload,
+		});
+		const secondResponse = caller.session.question.respond({
+			sessionId: SESSION_ID,
+			cwd: CWD,
+			payload,
+		});
+
+		await new Promise((resolve) => setTimeout(resolve, 0));
+
+		expect(respondToQuestion).toHaveBeenCalledTimes(1);
+		expect(runtime.answeredQuestionIds.has("sandbox-1")).toBe(true);
+		expect(runtime.pendingSandboxQuestion).toBeNull();
+
+		resolveResponse({ ok: true });
+
+		await expect(firstResponse).resolves.toEqual({ ok: true });
+		await expect(secondResponse).resolves.toEqual({ ok: true });
+		expect(runtime.pendingQuestionResponses.size).toBe(0);
+	});
 });
diff --git a/packages/chat/src/server/trpc/service.ts b/packages/chat/src/server/trpc/service.ts
index b173061c742..8299f9b29ee 100644
--- a/packages/chat/src/server/trpc/service.ts
+++ b/packages/chat/src/server/trpc/service.ts
@@ -11,6 +11,7 @@ import {
 	getRuntimeMcpOverview,
 	type LifecycleEvent,
 	onUserPromptSubmit,
+	type RuntimeQuestionResponse,
 	type RuntimeSession,
 	reloadHookConfig,
 	restartRuntimeFromUserMessage,
@@ -35,6 +36,55 @@ import {
 
 const ENABLE_MASTRA_MCP_SERVERS = false;
 
+type RuntimeQuestionPayload = Parameters<
+	RuntimeSession["harness"]["respondToQuestion"]
+>[0];
+
+function respondToQuestionWithOptimisticState(
+	runtime: RuntimeSession,
+	payload: RuntimeQuestionPayload,
+): Promise<RuntimeQuestionResponse> {
+	const questionId = payload.questionId;
+	const pendingResponse = runtime.pendingQuestionResponses.get(questionId);
+	if (pendingResponse) return pendingResponse;
+
+	const wasAlreadyAnswered = runtime.answeredQuestionIds.has(questionId);
+	const previousSandboxQuestion = runtime.pendingSandboxQuestion;
+	const clearsSandboxQuestion =
+		previousSandboxQuestion?.questionId === questionId;
+
+	runtime.answeredQuestionIds.add(questionId);
+	if (clearsSandboxQuestion) {
+		runtime.pendingSandboxQuestion = null;
+	}
+
+	let responsePromise: Promise<RuntimeQuestionResponse>;
+	responsePromise = Promise.resolve()
+		.then(() => runtime.harness.respondToQuestion(payload))
+		.catch((error) => {
+			if (
+				runtime.pendingQuestionResponses.get(questionId) === responsePromise
+			) {
+				if (!wasAlreadyAnswered) {
+					runtime.answeredQuestionIds.delete(questionId);
+				}
+				if (clearsSandboxQuestion && runtime.pendingSandboxQuestion === null) {
+					runtime.pendingSandboxQuestion = previousSandboxQuestion;
+				}
+			}
+			throw error;
+		})
+		.finally(() => {
+			if (
+				runtime.pendingQuestionResponses.get(questionId) === responsePromise
+			) {
+				runtime.pendingQuestionResponses.delete(questionId);
+			}
+		});
+	runtime.pendingQuestionResponses.set(questionId, responsePromise);
+	return responsePromise;
+}
+
 function resolveOmModelFromAuth(): string | undefined {
 	if (process.env.GOOGLE_GENERATIVE_AI_API_KEY)
 		return "google/gemini-2.5-flash";
@@ -141,6 +191,8 @@ export class ChatRuntimeService {
 					mcpManualStatuses: new Map(),
 					lastErrorMessage: null,
 					pendingSandboxQuestion: null,
+					answeredQuestionIds: new Set(),
+					pendingQuestionResponses: new Map(),
 					cwd: runtimeCwd,
 				};
 				syncRuntimeHookSessionId(sessionRuntime);
@@ -225,22 +277,30 @@ export class ChatRuntimeService {
 							? {
 									questionId: runtime.pendingSandboxQuestion.questionId,
 									question: `Grant sandbox access to "${runtime.pendingSandboxQuestion.path}"?`,
+									description: runtime.pendingSandboxQuestion.reason,
 									options: [
 										{
 											label: "Yes",
-											description: `Allow access. Reason: ${runtime.pendingSandboxQuestion.reason}`,
-										},
-										{
-											label: "No",
-											description: "Deny access.",
+											description: "Allow access.",
 										},
+										{ label: "No", description: "Deny access." },
 									],
 								}
 							: null;
+						// Skip any pending question whose ID was already answered this turn.
+						// The harness only clears pendingQuestion on agent_end, so without this
+						// filter an answered ask_user question would permanently shadow the
+						// sandbox question that fired in the same turn.
+						const harnessPendingQuestion =
+							displayState.pendingQuestion &&
+							!runtime.answeredQuestionIds.has(
+								displayState.pendingQuestion.questionId,
+							)
+								? displayState.pendingQuestion
+								: null;
 						return {
 							...displayState,
-							pendingQuestion:
-								displayState.pendingQuestion ?? sandboxPendingQuestion,
+							pendingQuestion: harnessPendingQuestion ?? sandboxPendingQuestion,
 							errorMessage: currentMessageError ?? runtime.lastErrorMessage,
 						};
 					}),
@@ -348,13 +408,10 @@ export class ChatRuntimeService {
 								input.sessionId,
 								input.cwd,
 							);
-							if (
-								runtime.pendingSandboxQuestion?.questionId ===
-								input.payload.questionId
-							) {
-								runtime.pendingSandboxQuestion = null;
-							}
-							return runtime.harness.respondToQuestion(input.payload);
+							return respondToQuestionWithOptimisticState(
+								runtime,
+								input.payload,
+							);
 						}),
 				}),
 
diff --git a/packages/chat/src/server/trpc/utils/runtime/index.ts b/packages/chat/src/server/trpc/utils/runtime/index.ts
index 3ebd1de45e0..d3dc1dd02f6 100644
--- a/packages/chat/src/server/trpc/utils/runtime/index.ts
+++ b/packages/chat/src/server/trpc/utils/runtime/index.ts
@@ -7,6 +7,7 @@ export {
 	type RuntimeHookManager,
 	type RuntimeMcpManager,
 	type RuntimeMcpServerStatus,
+	type RuntimeQuestionResponse,
 	type RuntimeSession,
 	reloadHookConfig,
 	restartRuntimeFromUserMessage,
diff --git a/packages/chat/src/server/trpc/utils/runtime/runtime.test.ts b/packages/chat/src/server/trpc/utils/runtime/runtime.test.ts
index 0327f0bf5ad..d93acb70520 100644
--- a/packages/chat/src/server/trpc/utils/runtime/runtime.test.ts
+++ b/packages/chat/src/server/trpc/utils/runtime/runtime.test.ts
@@ -55,6 +55,8 @@ function createRuntimeForTest(): {
 		mcpManualStatuses: new Map(),
 		lastErrorMessage: null,
 		pendingSandboxQuestion: null,
+		answeredQuestionIds: new Set(),
+		pendingQuestionResponses: new Map(),
 		cwd: "/tmp",
 	};
 
@@ -103,6 +105,8 @@ function createRuntimeForTitleTest(options?: {
 		mcpManualStatuses: new Map(),
 		lastErrorMessage: null,
 		pendingSandboxQuestion: null,
+		answeredQuestionIds: new Set(),
+		pendingQuestionResponses: new Map(),
 		cwd: "/tmp",
 	};
 
@@ -339,6 +343,8 @@ describe("runtime message restart", () => {
 			mcpManualStatuses: new Map(),
 			lastErrorMessage: "stale error",
 			pendingSandboxQuestion: null,
+			answeredQuestionIds: new Set(),
+			pendingQuestionResponses: new Map(),
 			cwd: "/tmp",
 		};
 
diff --git a/packages/chat/src/server/trpc/utils/runtime/runtime.ts b/packages/chat/src/server/trpc/utils/runtime/runtime.ts
index 905ec9ef8ef..2b1143693fb 100644
--- a/packages/chat/src/server/trpc/utils/runtime/runtime.ts
+++ b/packages/chat/src/server/trpc/utils/runtime/runtime.ts
@@ -13,6 +13,9 @@ export type RuntimeMcpManager = Awaited<
 export type RuntimeHookManager = Awaited<
 	ReturnType<typeof createMastraCode>
 >["hookManager"];
+export type RuntimeQuestionResponse = Awaited<
+	ReturnType<RuntimeHarness["respondToQuestion"]>
+>;
 
 export interface RuntimeMcpServerStatus {
 	connected: boolean;
@@ -32,6 +35,8 @@ export interface RuntimeSession {
 		path: string;
 		reason: string;
 	} | null;
+	answeredQuestionIds: Set<string>;
+	pendingQuestionResponses: Map<string, Promise<RuntimeQuestionResponse>>;
 	cwd: string;
 }
 
@@ -224,6 +229,8 @@ export function subscribeToSessionEvents(
 		if (isHarnessAgentStartEvent(event)) {
 			runtime.lastErrorMessage = null;
 			runtime.pendingSandboxQuestion = null;
+			runtime.answeredQuestionIds.clear();
+			runtime.pendingQuestionResponses.clear();
 			onLifecycleEvent?.({
 				sessionId: runtime.sessionId,
 				eventType: "Start",
@@ -232,6 +239,8 @@ export function subscribeToSessionEvents(
 		}
 		if (isHarnessAgentEndEvent(event)) {
 			runtime.pendingSandboxQuestion = null;
+			runtime.answeredQuestionIds.clear();
+			runtime.pendingQuestionResponses.clear();
 			const raw = event.reason;
 			const reason = raw === "aborted" || raw === "error" ? raw : "complete";
 			if (runtime.hookManager) {
diff --git a/packages/host-service/src/runtime/chat/chat.ts b/packages/host-service/src/runtime/chat/chat.ts
index a25c253ecb6..514fb3871c3 100644
--- a/packages/host-service/src/runtime/chat/chat.ts
+++ b/packages/host-service/src/runtime/chat/chat.ts
@@ -59,12 +59,13 @@ interface PendingSandboxQuestion {
 
 interface ChatPendingQuestionOption {
 	label: string;
-	description: string;
+	description?: string;
 }
 
 interface ChatPendingQuestion {
 	questionId: string;
 	question: string;
+	description?: string;
 	options: ChatPendingQuestionOption[];
 }
 
@@ -102,6 +103,53 @@ interface RuntimeSession {
 	hookManager: RuntimeHookManager;
 	lastErrorMessage: string | null;
 	pendingSandboxQuestion: PendingSandboxQuestion | null;
+	answeredQuestionIds: Set<string>;
+	pendingQuestionResponses: Map<string, Promise<RuntimeQuestionResult>>;
+}
+
+function respondToQuestionWithOptimisticState(
+	runtime: RuntimeSession,
+	payload: ChatQuestionPayload,
+): Promise<RuntimeQuestionResult> {
+	const questionId = payload.questionId;
+	const pendingResponse = runtime.pendingQuestionResponses.get(questionId);
+	if (pendingResponse) return pendingResponse;
+
+	const wasAlreadyAnswered = runtime.answeredQuestionIds.has(questionId);
+	const previousSandboxQuestion = runtime.pendingSandboxQuestion;
+	const clearsSandboxQuestion =
+		previousSandboxQuestion?.questionId === questionId;
+
+	runtime.answeredQuestionIds.add(questionId);
+	if (clearsSandboxQuestion) {
+		runtime.pendingSandboxQuestion = null;
+	}
+
+	let responsePromise: Promise<RuntimeQuestionResult>;
+	responsePromise = Promise.resolve()
+		.then(() => runtime.harness.respondToQuestion(payload))
+		.catch((error) => {
+			if (
+				runtime.pendingQuestionResponses.get(questionId) === responsePromise
+			) {
+				if (!wasAlreadyAnswered) {
+					runtime.answeredQuestionIds.delete(questionId);
+				}
+				if (clearsSandboxQuestion && runtime.pendingSandboxQuestion === null) {
+					runtime.pendingSandboxQuestion = previousSandboxQuestion;
+				}
+			}
+			throw error;
+		})
+		.finally(() => {
+			if (
+				runtime.pendingQuestionResponses.get(questionId) === responsePromise
+			) {
+				runtime.pendingQuestionResponses.delete(questionId);
+			}
+		});
+	runtime.pendingQuestionResponses.set(questionId, responsePromise);
+	return responsePromise;
 }
 
 interface RuntimeStoredMessage {
@@ -342,11 +390,15 @@ export class ChatRuntimeManager {
 			if (isObjectRecord(event) && event.type === "agent_start") {
 				runtime.lastErrorMessage = null;
 				runtime.pendingSandboxQuestion = null;
+				runtime.answeredQuestionIds.clear();
+				runtime.pendingQuestionResponses.clear();
 				return;
 			}
 
 			if (isObjectRecord(event) && event.type === "agent_end") {
 				runtime.pendingSandboxQuestion = null;
+				runtime.answeredQuestionIds.clear();
+				runtime.pendingQuestionResponses.clear();
 			}
 		});
 	}
@@ -419,6 +471,8 @@ When you need to ask the user ANY question — including simple yes/no, confirma
 			hookManager: runtime.hookManager,
 			lastErrorMessage: null,
 			pendingSandboxQuestion: null,
+			answeredQuestionIds: new Set(),
+			pendingQuestionResponses: new Map(),
 		};
 		this.subscribeToSessionEvents(sessionRuntime);
 		this.runtimes.set(sessionId, sessionRuntime);
@@ -471,26 +525,32 @@ When you need to ask the user ANY question — including simple yes/no, confirma
 				? currentMessage.errorMessage.trim()
 				: null;
 
+		// Skip any pending question whose ID was already answered this turn.
+		// The harness only clears pendingQuestion on agent_end, so without this
+		// filter an answered ask_user question would permanently shadow the
+		// sandbox question that fired in the same turn.
+		const harnessPendingQuestion =
+			displayState.pendingQuestion &&
+			!runtime.answeredQuestionIds.has(displayState.pendingQuestion.questionId)
+				? displayState.pendingQuestion
+				: null;
+		const sandboxPendingQuestion = runtime.pendingSandboxQuestion
+			? {
+					questionId: runtime.pendingSandboxQuestion.questionId,
+					question: `Grant sandbox access to "${runtime.pendingSandboxQuestion.path}"?`,
+					description: runtime.pendingSandboxQuestion.reason,
+					options: [
+						{
+							label: "Yes",
+							description: "Allow access.",
+						},
+						{ label: "No", description: "Deny access." },
+					],
+				}
+			: null;
 		return {
 			...displayState,
-			pendingQuestion:
-				displayState.pendingQuestion ??
-				(runtime.pendingSandboxQuestion
-					? {
-							questionId: runtime.pendingSandboxQuestion.questionId,
-							question: `Grant sandbox access to "${runtime.pendingSandboxQuestion.path}"?`,
-							options: [
-								{
-									label: "Yes",
-									description: `Allow access. Reason: ${runtime.pendingSandboxQuestion.reason}`,
-								},
-								{
-									label: "No",
-									description: "Deny access.",
-								},
-							],
-						}
-					: null),
+			pendingQuestion: harnessPendingQuestion ?? sandboxPendingQuestion,
 			errorMessage: currentMessageError ?? runtime.lastErrorMessage,
 		};
 	}
@@ -570,13 +630,7 @@ When you need to ask the user ANY question — including simple yes/no, confirma
 			input.workspaceId,
 		);
 
-		if (
-			runtime.pendingSandboxQuestion?.questionId === input.payload.questionId
-		) {
-			runtime.pendingSandboxQuestion = null;
-		}
-
-		return runtime.harness.respondToQuestion(input.payload);
+		return respondToQuestionWithOptimisticState(runtime, input.payload);
 	}
 
 	async respondToPlan(input: {