diff --git a/site/src/pages/AgentsPage/components/AgentChatInput.tsx b/site/src/pages/AgentsPage/components/AgentChatInput.tsx
index ca4fdfd20b..95bc30e904 100644
--- a/site/src/pages/AgentsPage/components/AgentChatInput.tsx
+++ b/site/src/pages/AgentsPage/components/AgentChatInput.tsx
@@ -137,6 +137,7 @@ interface AgentChatInputProps {
 	// History editing state, owned by the parent.
 	isEditingHistoryMessage?: boolean;
 	onCancelHistoryEdit?: () => void;
+	onEditLastUserMessage?: () => void;
 
 	// Optional context-usage summary shown to the left of the send button.
 	// Pass `null` to render fallback values (e.g. when limit is unknown).
@@ -547,6 +548,7 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 	onCancelQueueEdit,
 	isEditingHistoryMessage = false,
 	onCancelHistoryEdit,
+	onEditLastUserMessage,
 	contextUsage,
 	attachments = [],
 	onAttach,
@@ -774,11 +776,16 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 	const hasUploadedAttachments = attachments.some(
 		(f) => uploadStates?.get(f)?.status === "uploaded",
 	);
+	const hasDraftContext =
+		hasContent || attachments.length > 0 || hasFileReferences;
+	const isComposerEffectivelyEmpty = !hasDraftContext;
+	const hasSendableContent =
+		hasContent || hasUploadedAttachments || hasFileReferences;
 	const canSend =
 		!isDisabled &&
 		!isLoading &&
 		hasModelOptions &&
-		(hasContent || hasUploadedAttachments || hasFileReferences) &&
+		hasSendableContent &&
 		!isUploading;
 	const handleSubmit = () => {
 		const text = internalRef.current?.getValue()?.trim() ?? "";
@@ -836,7 +843,7 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 		setPreRecordingValue("");
 	};
 
-	const handleKeyDown = (e: React.KeyboardEvent) => {
+	const handleComposerKeyDown = (e: React.KeyboardEvent) => {
 		if (e.key === "Escape") {
 			if (editingQueuedMessageID !== null) {
 				e.preventDefault();
@@ -850,6 +857,19 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 			}
 		}
 	};
+	const handleEditorKeyDown = (e: React.KeyboardEvent) => {
+		if (
+			e.key !== "ArrowUp" ||
+			editingQueuedMessageID !== null ||
+			isEditingHistoryMessage ||
+			!onEditLastUserMessage ||
+			!isComposerEffectivelyEmpty
+		) {
+			return;
+		}
+		e.preventDefault();
+		onEditLastUserMessage();
+	};
 
 	const sendButtonLabel =
 		editingQueuedMessageID !== null
@@ -892,7 +912,7 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 					isEditingHistoryMessage &&
 						"shadow-[0_0_0_2px_hsla(var(--border-warning),0.6)]",
 				)}
-				onKeyDown={handleKeyDown}
+				onKeyDown={handleComposerKeyDown}
 				onDragOver={onAttach ? handleDragOver : undefined}
 				onDragLeave={onAttach ? handleDragLeave : undefined}
 				onDrop={onAttach ? handleDrop : undefined}
@@ -954,6 +974,7 @@ export const AgentChatInput: FC<AgentChatInputProps> = ({
 					placeholder={placeholder}
 					initialValue={initialValue}
 					onChange={handleContentChange}
+					onKeyDown={handleEditorKeyDown}
 					onEnter={handleSubmit}
 					disabled={isDisabled || isLoading}
 					autoFocus
diff --git a/site/src/pages/AgentsPage/components/AgentDetail/ConversationTimeline.tsx b/site/src/pages/AgentsPage/components/AgentDetail/ConversationTimeline.tsx
index 7db618dc4c..fd08fdec97 100644
--- a/site/src/pages/AgentsPage/components/AgentDetail/ConversationTimeline.tsx
+++ b/site/src/pages/AgentsPage/components/AgentDetail/ConversationTimeline.tsx
@@ -37,7 +37,10 @@ import { ImageLightbox } from "../ImageLightbox";
 import { TextPreviewDialog } from "../TextPreviewDialog";
 import { ChatStatusCallout } from "./ChatStatusCallout";
 import type { LiveStatusModel } from "./liveStatusModel";
-import { buildSubagentTitles } from "./messageParsing";
+import {
+	buildSubagentTitles,
+	getEditableUserMessagePayload,
+} from "./messageParsing";
 import { useSmoothStreamingText } from "./SmoothText";
 import type {
 	MergedTool,
@@ -565,24 +568,9 @@ const ChatMessageItem = memo<{
 															className="mt-0.5 inline-flex size-6 shrink-0 cursor-pointer items-center justify-center rounded-md border-none bg-transparent p-0 text-content-secondary opacity-0 transition-opacity hover:bg-surface-tertiary hover:text-content-primary focus-visible:opacity-100 focus-visible:outline-none focus-visible:ring-2 focus-visible:ring-content-link group-hover/msg:opacity-100"
 															aria-label="Edit message"
 															onClick={() => {
-																const fileBlocks = parsed.blocks.filter(
-																	(
-																		b,
-																	): b is Extract<
-																		RenderBlock,
-																		{ type: "file" }
-																	> =>
-																		b.type === "file" &&
-																		(b.media_type.startsWith("image/") ||
-																			b.media_type === "text/plain"),
-																);
-																onEditUserMessage(
-																	message.id,
-																	parsed.markdown || "",
-																	fileBlocks.length > 0
-																		? fileBlocks
-																		: undefined,
-																);
+																const { text, fileBlocks } =
+																	getEditableUserMessagePayload(message);
+																onEditUserMessage(message.id, text, fileBlocks);
 															}}
 														>
 															<PencilIcon className="size-3.5" />
diff --git a/site/src/pages/AgentsPage/components/AgentDetail/messageParsing.ts b/site/src/pages/AgentsPage/components/AgentDetail/messageParsing.ts
index 762f3adf8d..8b3b43463a 100644
--- a/site/src/pages/AgentsPage/components/AgentDetail/messageParsing.ts
+++ b/site/src/pages/AgentsPage/components/AgentDetail/messageParsing.ts
@@ -224,6 +224,26 @@ export const parseMessageContent = (
 	return parsed;
 };
 
+const isEditableUserMessageFileBlock = (
+	block: RenderBlock,
+): block is TypesGen.ChatFilePart =>
+	block.type === "file" &&
+	(block.media_type.startsWith("image/") || block.media_type === "text/plain");
+
+export const getEditableUserMessagePayload = (
+	message: TypesGen.ChatMessage,
+): {
+	text: string;
+	fileBlocks: readonly TypesGen.ChatMessagePart[] | undefined;
+} => {
+	const parsed = parseMessageContent(message.content);
+	const fileBlocks = parsed.blocks.filter(isEditableUserMessageFileBlock);
+	return {
+		text: parsed.markdown || "",
+		fileBlocks: fileBlocks.length > 0 ? fileBlocks : undefined,
+	};
+};
+
 export const parseMessagesWithMergedTools = (
 	messages: readonly TypesGen.ChatMessage[],
 ): ParsedMessageEntry[] => {
diff --git a/site/src/pages/AgentsPage/components/AgentDetailContent.tsx b/site/src/pages/AgentsPage/components/AgentDetailContent.tsx
index c75088c244..0225262870 100644
--- a/site/src/pages/AgentsPage/components/AgentDetailContent.tsx
+++ b/site/src/pages/AgentsPage/components/AgentDetailContent.tsx
@@ -26,6 +26,7 @@ import { LiveStreamTail } from "./AgentDetail/LiveStreamTail";
 import {
 	buildComputerUseSubagentIds,
 	buildSubagentTitles,
+	getEditableUserMessagePayload,
 	parseMessagesWithMergedTools,
 } from "./AgentDetail/messageParsing";
 import { useOnRenderProfiler } from "./AgentDetail/useOnRenderProfiler";
@@ -135,6 +136,11 @@ interface AgentDetailInputProps {
 	onCancelQueueEdit: () => void;
 	isEditingHistoryMessage: boolean;
 	onCancelHistoryEdit: () => void;
+	onEditUserMessage: (
+		messageId: number,
+		text: string,
+		fileBlocks?: readonly TypesGen.ChatMessagePart[],
+	) => void;
 	// File parts from the message being edited, converted to
 	// File objects and pre-populated into attachments.
 	editingFileBlocks?: readonly TypesGen.ChatMessagePart[];
@@ -169,6 +175,7 @@ export const AgentDetailInput: FC<AgentDetailInputProps> = ({
 	onCancelQueueEdit,
 	isEditingHistoryMessage,
 	onCancelHistoryEdit,
+	onEditUserMessage,
 	editingFileBlocks,
 	mcpServers,
 	selectedMCPServerIds,
@@ -184,6 +191,24 @@ export const AgentDetailInput: FC<AgentDetailInputProps> = ({
 	const messages = orderedMessageIDs
 		.map((messageID) => messagesByID.get(messageID))
 		.filter(isChatMessage);
+	let lastEditableUserMessage: TypesGen.ChatMessage | undefined;
+	for (let index = orderedMessageIDs.length - 1; index >= 0; index--) {
+		const message = messagesByID.get(orderedMessageIDs[index]);
+		if (message?.role === "user") {
+			lastEditableUserMessage = message;
+			break;
+		}
+	}
+
+	const handleEditLastUserMessage = lastEditableUserMessage
+		? () => {
+				const { text, fileBlocks } = getEditableUserMessagePayload(
+					lastEditableUserMessage,
+				);
+				onEditUserMessage(lastEditableUserMessage.id, text, fileBlocks);
+			}
+		: undefined;
+
 	const rawUsage = getLatestContextUsage(messages);
 	const latestContextUsage = rawUsage
 		? { ...rawUsage, compressionThreshold }
@@ -297,6 +322,7 @@ export const AgentDetailInput: FC<AgentDetailInputProps> = ({
 			onCancelQueueEdit={onCancelQueueEdit}
 			isEditingHistoryMessage={isEditingHistoryMessage}
 			onCancelHistoryEdit={onCancelHistoryEdit}
+			onEditLastUserMessage={handleEditLastUserMessage}
 			isDisabled={isInputDisabled}
 			isLoading={isSendPending}
 			isStreaming={isStreaming}
diff --git a/site/src/pages/AgentsPage/components/AgentDetailView.tsx b/site/src/pages/AgentsPage/components/AgentDetailView.tsx
index fd3ff693a4..7e605d2add 100644
--- a/site/src/pages/AgentsPage/components/AgentDetailView.tsx
+++ b/site/src/pages/AgentsPage/components/AgentDetailView.tsx
@@ -340,6 +340,7 @@ export const AgentDetailView: FC<AgentDetailViewProps> = ({
 							onCancelQueueEdit={editing.handleCancelQueueEdit}
 							isEditingHistoryMessage={editing.editingMessageId !== null}
 							onCancelHistoryEdit={editing.handleCancelHistoryEdit}
+							onEditUserMessage={editing.handleEditUserMessage}
 							editingFileBlocks={editing.editingFileBlocks}
 							mcpServers={mcpServers}
 							selectedMCPServerIds={selectedMCPServerIds}