diff --git a/site/src/components/ChatMessageInput/FileReferenceNode.tsx b/site/src/components/ChatMessageInput/FileReferenceNode.tsx
index e735948e72..0ab0196084 100644
--- a/site/src/components/ChatMessageInput/FileReferenceNode.tsx
+++ b/site/src/components/ChatMessageInput/FileReferenceNode.tsx
@@ -23,7 +23,7 @@ type SerializedFileReferenceNode = Spread<
 	SerializedLexicalNode
 >;
 
-function FileReferenceChip({
+export function FileReferenceChip({
 	fileName,
 	startLine,
 	endLine,
@@ -35,7 +35,7 @@ function FileReferenceChip({
 	startLine: number;
 	endLine: number;
 	isSelected?: boolean;
-	onRemove: () => void;
+	onRemove?: () => void;
 	onClick?: () => void;
 }) {
 	const shortFile = fileName.split("/").pop() || fileName;
@@ -66,19 +66,21 @@ function FileReferenceChip({
 				{shortFile}
 				<span className="text-content-link">:{lineLabel}</span>
 			</span>
-			<button
-				type="button"
-				className="ml-auto inline-flex size-4 shrink-0 items-center justify-center rounded border-0 bg-transparent p-0 text-content-secondary transition-colors hover:text-content-primary cursor-pointer"
-				onClick={(e) => {
-					e.preventDefault();
-					e.stopPropagation();
-					onRemove();
-				}}
-				aria-label="Remove reference"
-				tabIndex={-1}
-			>
-				<XIcon className="size-2" />
-			</button>
+			{onRemove && (
+				<button
+					type="button"
+					className="ml-auto inline-flex size-4 shrink-0 items-center justify-center rounded border-0 bg-transparent p-0 text-content-secondary transition-colors hover:text-content-primary cursor-pointer"
+					onClick={(e) => {
+						e.preventDefault();
+						e.stopPropagation();
+						onRemove();
+					}}
+					aria-label="Remove reference"
+					tabIndex={-1}
+				>
+					<XIcon className="size-2" />
+				</button>
+			)}
 		</span>
 	);
 }
diff --git a/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.stories.tsx b/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.stories.tsx
index 4d7470ee2b..c59e3b2a99 100644
--- a/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.stories.tsx
+++ b/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.stories.tsx
@@ -244,3 +244,79 @@ export const UserMessageWithImagesAndFileRefs: Story = {
 		expect(canvas.getByText(/main\.go/)).toBeInTheDocument();
 	},
 };
+
+/** File references render inline with text, matching the chat input style. */
+export const UserMessageWithInlineFileRef: Story = {
+	args: {
+		...defaultArgs,
+		parsedSections: buildSections([
+			{
+				...baseMessage,
+				id: 1,
+				role: "user",
+				content: [
+					{ type: "text", text: "Can you refactor " },
+					{
+						type: "file-reference",
+						file_name: "site/src/components/Button.tsx",
+						start_line: 42,
+						end_line: 42,
+						content: "export const Button = ...",
+					},
+					{ type: "text", text: " to use the new API?" },
+				],
+			},
+			{
+				...baseMessage,
+				id: 2,
+				role: "assistant",
+				content: [{ type: "text", text: "Sure, I'll update that component." }],
+			},
+		]),
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		// File ref chip is inline, rendered as a button
+		expect(canvas.getByText(/Button\.tsx/)).toBeInTheDocument();
+		// Surrounding text is present
+		expect(canvas.getByText(/Can you refactor/)).toBeInTheDocument();
+		expect(canvas.getByText(/to use the new API/)).toBeInTheDocument();
+	},
+};
+
+/** Multiple file references render inline, no separate section. */
+export const UserMessageWithMultipleInlineFileRefs: Story = {
+	args: {
+		...defaultArgs,
+		parsedSections: buildSections([
+			{
+				...baseMessage,
+				id: 1,
+				role: "user",
+				content: [
+					{ type: "text", text: "Compare " },
+					{
+						type: "file-reference",
+						file_name: "api/handler.go",
+						start_line: 1,
+						end_line: 50,
+						content: "...",
+					},
+					{ type: "text", text: " with " },
+					{
+						type: "file-reference",
+						file_name: "api/handler_test.go",
+						start_line: 10,
+						end_line: 30,
+						content: "...",
+					},
+				],
+			},
+		]),
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		expect(canvas.getByText(/handler\.go/)).toBeInTheDocument();
+		expect(canvas.getByText(/handler_test\.go/)).toBeInTheDocument();
+	},
+};
diff --git a/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.tsx b/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.tsx
index 401b598f18..eff6c3d9b9 100644
--- a/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.tsx
+++ b/site/src/pages/AgentsPage/AgentDetail/ConversationTimeline.tsx
@@ -8,11 +8,12 @@ import {
 	Tool,
 } from "components/ai-elements";
 import { WebSearchSources } from "components/ai-elements/tool";
-import { FileIcon } from "components/FileIcon/FileIcon";
+import { FileReferenceChip } from "components/ChatMessageInput/FileReferenceNode";
 import { Spinner } from "components/Spinner/Spinner";
 import { ChevronDownIcon } from "lucide-react";
 import {
 	type FC,
+	Fragment,
 	memo,
 	type ReactNode,
 	type RefObject,
@@ -337,6 +338,20 @@ const ChatMessageItem = memo<{
 			parsed.blocks.length > 0 ||
 			parsed.tools.length > 0 ||
 			parsed.sources.length > 0;
+
+		// Pre-compute the inline content for user messages so we
+		// avoid a filter + map inside the JSX return path.
+		const userInlineContent = isUser
+			? parsed.blocks.filter(
+					(
+						b,
+					): b is
+						| Extract<RenderBlock, { type: "response" }>
+						| Extract<RenderBlock, { type: "file-reference" }> =>
+						b.type === "response" || b.type === "file-reference",
+				)
+			: [];
+
 		const conversationItemProps: { role: "user" | "assistant" } = {
 			role: isUser ? "user" : "assistant",
 		};
@@ -392,7 +407,20 @@ const ChatMessageItem = memo<{
 								<div className="flex flex-col gap-1.5">
 									<div className="flex items-start gap-2">
 										<span className="min-w-0 flex-1">
-											{parsed.markdown || ""}
+											{userInlineContent.length > 0
+												? userInlineContent.map((block, i) =>
+														block.type === "response" ? (
+															<Fragment key={i}>{block.text}</Fragment>
+														) : (
+															<FileReferenceChip
+																key={i}
+																fileName={block.fileName}
+																startLine={block.startLine}
+																endLine={block.endLine}
+															/>
+														),
+													)
+												: parsed.markdown || ""}
 										</span>
 										{isSavingMessage && (
 											<Spinner
@@ -435,45 +463,7 @@ const ChatMessageItem = memo<{
 											</div>
 										);
 									})()}
-									{(() => {
-										const fileRefBlocks = parsed.blocks.filter(
-											(
-												b,
-											): b is Extract<
-												RenderBlock,
-												{ type: "file-reference" }
-											> => b.type === "file-reference",
-										);
-										if (fileRefBlocks.length === 0) return null;
-										return (
-											<div className="flex flex-col gap-1 border-t border-border-default pt-1.5">
-												{fileRefBlocks.map((dc, i) => (
-													<div
-														key={i}
-														className="flex items-start gap-2 rounded border border-content-link/20 bg-content-link/5 px-2 py-1"
-													>
-														<FileIcon
-															fileName={
-																dc.fileName.split("/").pop() || dc.fileName
-															}
-															className="shrink-0"
-														/>
-														<span className="shrink-0 text-2xs font-mono font-medium text-content-link">
-															{dc.fileName.split("/").pop()}:
-															{dc.startLine === dc.endLine
-																? dc.startLine
-																: `${dc.startLine}\u2013${dc.endLine}`}
-														</span>
-														{dc.text && (
-															<span className="text-2xs text-content-primary">
-																{dc.text}
-															</span>
-														)}
-													</div>
-												))}
-											</div>
-										);
-									})()} {fadeFromBottom && (
+									{fadeFromBottom && (
 										<div
 											className="pointer-events-none absolute inset-x-0 bottom-0 h-1/2 max-h-12"
 											style={{