diff --git a/site/src/components/ChatMessageInput/ChatMessageInput.tsx b/site/src/components/ChatMessageInput/ChatMessageInput.tsx
index 02526da890..23ad9c3c31 100644
--- a/site/src/components/ChatMessageInput/ChatMessageInput.tsx
+++ b/site/src/components/ChatMessageInput/ChatMessageInput.tsx
@@ -27,6 +27,7 @@ import {
 	useCallback,
 	useEffect,
 	useImperativeHandle,
+	useLayoutEffect,
 	useMemo,
 	useRef,
 } from "react";
@@ -221,6 +222,21 @@ interface ChatMessageInputProps
 	"aria-label"?: string;
 }
 
+// Keeps the Lexical editor's editable state in sync with the
+// disabled prop so that the underlying contentEditable element
+// becomes truly non-interactive when the input is disabled.
+const EditableStatePlugin: FC<{ disabled: boolean }> = memo(
+	function EditableStatePlugin({ disabled }) {
+		const [editor] = useLexicalComposerContext();
+
+		useLayoutEffect(() => {
+			editor.setEditable(!disabled);
+		}, [editor, disabled]);
+
+		return null;
+	},
+);
+
 const ChatMessageInput = memo(
 	({
 		className,
@@ -243,8 +259,9 @@ const ChatMessageInput = memo(
 				},
 				onError: (error: Error) => console.error("Lexical error:", error),
 				nodes: [],
+				editable: !disabled,
 			}),
-			[],
+			[disabled],
 		);
 		const style = useMemo(
 			() => ({
@@ -380,6 +397,7 @@ const ChatMessageInput = memo(
 					<ContentChangePlugin onChange={handleContentChange} />
 					<ValueSyncPlugin initialValue={initialValue} />
 					<InsertTextPlugin onEditorReady={handleEditorReady} />
+					<EditableStatePlugin disabled={!!disabled} />
 					{autoFocus && <AutoFocusPlugin />}
 				</div>
 			</LexicalComposer>
diff --git a/site/src/pages/AgentsPage/AgentChatInput.stories.tsx b/site/src/pages/AgentsPage/AgentChatInput.stories.tsx
index ee891280ff..7f3a287e6f 100644
--- a/site/src/pages/AgentsPage/AgentChatInput.stories.tsx
+++ b/site/src/pages/AgentsPage/AgentChatInput.stories.tsx
@@ -80,6 +80,13 @@ export const DisabledInput: Story = {
 	play: async ({ canvasElement }) => {
 		const canvas = within(canvasElement);
 		expect(canvas.getByRole("button", { name: "Send" })).toBeDisabled();
+
+		// The editor should be non-editable so users cannot click
+		// into it and type (e.g. archived chats).
+		const editor = canvas.getByTestId("chat-message-input");
+		await waitFor(() => {
+			expect(editor).toHaveAttribute("contenteditable", "false");
+		});
 	},
 };