diff --git a/site/src/pages/AgentsPage/AgentsSidebar.stories.tsx b/site/src/pages/AgentsPage/AgentsSidebar.stories.tsx
index 275e64c30b..a2efccfea7 100644
--- a/site/src/pages/AgentsPage/AgentsSidebar.stories.tsx
+++ b/site/src/pages/AgentsPage/AgentsSidebar.stories.tsx
@@ -197,6 +197,49 @@ export const ExpandCollapse: Story = {
 	},
 };
 
+export const RunningChatPreservesSpinner: Story = {
+	args: {
+		chats: [
+			buildChat({
+				id: "root-running",
+				title: "Running root agent",
+				status: "running",
+			}),
+			buildChat({
+				id: "child-of-running",
+				title: "Child of running",
+				parent_chat_id: "root-running",
+				root_chat_id: "root-running",
+			}),
+		],
+	},
+	parameters: {
+		reactRouter: reactRouterParameters({
+			location: {
+				path: "/agents/child-of-running",
+				pathParams: { agentId: "child-of-running" },
+			},
+			routing: agentsRouting,
+		}),
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+
+		// The root chat is running and has children, so a spinning
+		// Loader2Icon should be rendered inside the icon wrapper.
+		const node = canvas.getByTestId("agents-tree-node-root-running");
+		const spinner = node.querySelector(".animate-spin");
+		await expect(spinner).toBeInTheDocument();
+
+		// The toggle button should exist (the node has children) but
+		// must be invisible by default — it only appears on hover of
+		// the icon area itself, not the whole row.
+		const toggle = canvas.getByTestId("agents-tree-toggle-root-running");
+		await expect(toggle).toBeInTheDocument();
+		await expect(toggle.className).toMatch(/\binvisible\b/);
+	},
+};
+
 export const ActiveChatAncestryExpanded: Story = {
 	args: {
 		chats: [
diff --git a/site/src/pages/AgentsPage/AgentsSidebar.tsx b/site/src/pages/AgentsPage/AgentsSidebar.tsx
index e5ed8e44b6..0969789c60 100644
--- a/site/src/pages/AgentsPage/AgentsSidebar.tsx
+++ b/site/src/pages/AgentsPage/AgentsSidebar.tsx
@@ -327,6 +327,7 @@ const ChatTreeNode = memo<ChatTreeNodeProps>(({ chat, isChildNode }) => {
 	}`;
 	const isArchivingThisChat = isArchiving && archivingChatId === chat.id;
 	const isExpanded = normalizedSearch ? true : (expandedById[chatID] ?? false);
+	const isExecuting = chat.status === "pending" || chat.status === "running";
 
 	return (
 		<div className="flex min-w-0 flex-col">
@@ -340,11 +341,21 @@ const ChatTreeNode = memo<ChatTreeNodeProps>(({ chat, isChildNode }) => {
 						"before:absolute before:-left-2.5 before:top-[17px] before:h-px before:w-2.5 before:bg-border-default/70",
 				)}
 			>
-				<div className="relative mt-1.5 h-5 w-5 shrink-0">
+				<div
+					className={cn(
+						"group/icon relative mt-1.5 h-5 w-5 shrink-0",
+						hasChildren && "cursor-pointer",
+					)}
+				>
 					<div
 						className={cn(
 							"flex h-5 w-5 items-center justify-center rounded-md",
-							hasChildren && "[@media(hover:hover)]:group-hover:invisible",
+							hasChildren &&
+								!isExecuting &&
+								"[@media(hover:hover)]:group-hover:invisible",
+							hasChildren &&
+								isExecuting &&
+								"[@media(hover:hover)]:group-hover/icon:invisible",
 						)}
 					>
 						<StatusIcon
@@ -361,7 +372,12 @@ const ChatTreeNode = memo<ChatTreeNodeProps>(({ chat, isChildNode }) => {
 							variant="subtle"
 							size="icon"
 							onClick={() => toggleExpanded(chatID)}
-							className="absolute inset-0 invisible flex h-5 w-5 min-w-0 items-center justify-center rounded-md p-0 text-content-secondary/60 hover:text-content-primary [@media(hover:hover)]:group-hover:visible [&>svg]:size-3.5"
+							className={cn(
+								"absolute inset-0 invisible flex h-5 w-5 min-w-0 items-center justify-center rounded-md p-0 text-content-secondary/60 hover:text-content-primary [&>svg]:size-3.5",
+								isExecuting
+									? "[@media(hover:hover)]:group-hover/icon:visible"
+									: "[@media(hover:hover)]:group-hover:visible",
+							)}
 							data-testid={`agents-tree-toggle-${chat.id}`}
 							aria-label={isExpanded ? "Collapse" : "Expand"}
 							aria-expanded={isExpanded}