diff --git a/site/src/pages/AgentsPage/components/ContextUsageIndicator.stories.tsx b/site/src/pages/AgentsPage/components/ContextUsageIndicator.stories.tsx
index 22b8c3ed58..50f29774f9 100644
--- a/site/src/pages/AgentsPage/components/ContextUsageIndicator.stories.tsx
+++ b/site/src/pages/AgentsPage/components/ContextUsageIndicator.stories.tsx
@@ -204,6 +204,65 @@ export const Dirty: Story = {
 	},
 };
 
+// Before any assistant message reports token usage there is no percentage,
+// so the popover explains when the numbers will appear.
+export const NoUsage: Story = {
+	args: {
+		usage: null,
+	},
+	play: async ({ canvasElement }) => {
+		const button = within(canvasElement).getByRole("button");
+		await userEvent.hover(button);
+		const body = within(document.body);
+		await waitFor(() =>
+			expect(
+				body.getByText("Context usage will appear after sending a message."),
+			).toBeVisible(),
+		);
+	},
+};
+
+// Some providers report usage without token counts, so no percentage can be
+// computed even though a message was sent. The popover must say the usage is
+// unavailable instead of promising numbers after the next message.
+export const UsageWithoutTokenCounts: Story = {
+	args: {
+		usage: {
+			contextLimitTokens: 200_000,
+		},
+	},
+	play: async ({ canvasElement }) => {
+		const button = within(canvasElement).getByRole("button");
+		await userEvent.hover(button);
+		const body = within(document.body);
+		await waitFor(() =>
+			expect(body.getByText("Context usage unavailable")).toBeVisible(),
+		);
+	},
+};
+
+// A fresh chat has pinned context before any assistant message reports token
+// usage, so the popover pairs the empty-usage copy with the resource list.
+export const NoUsageWithContext: Story = {
+	args: {
+		usage: {
+			context: MockChatContextClean,
+		},
+	},
+	play: async ({ canvasElement }) => {
+		const button = within(canvasElement).getByRole("button");
+		await userEvent.hover(button);
+		const body = within(document.body);
+		await waitFor(() =>
+			expect(
+				body.getByText("Context usage will appear after sending a message."),
+			).toBeVisible(),
+		);
+		expect(body.getByText("Context files")).toBeVisible();
+		expect(body.getByText("AGENTS.md")).toBeVisible();
+	},
+};
+
 // Snapshot-level error: the ring shows a distinct error treatment and the
 // popover surfaces the error message.
 export const SnapshotError: Story = {
diff --git a/site/src/pages/AgentsPage/components/ContextUsageIndicator.tsx b/site/src/pages/AgentsPage/components/ContextUsageIndicator.tsx
index 0111490ef4..f50a61c3b1 100644
--- a/site/src/pages/AgentsPage/components/ContextUsageIndicator.tsx
+++ b/site/src/pages/AgentsPage/components/ContextUsageIndicator.tsx
@@ -229,6 +229,17 @@ export const ContextUsageIndicator: FC<{
 			? (usedTokens / contextLimitTokens) * 100
 			: null;
 	const hasPercent = percentUsed !== null;
+	// Providers may report usage without token counts. Only a chat with no
+	// reported usage at all should promise numbers after the next message.
+	const hasReportedUsage = [
+		usage?.usedTokens,
+		usage?.contextLimitTokens,
+		usage?.inputTokens,
+		usage?.outputTokens,
+		usage?.cacheReadTokens,
+		usage?.cacheCreationTokens,
+		usage?.reasoningTokens,
+	].some(hasFiniteTokenValue);
 	const percentLabel =
 		percentUsed === null ? "--" : `${Math.round(percentUsed)}%`;
 	const clampedPercent = hasPercent
@@ -337,7 +348,9 @@ export const ContextUsageIndicator: FC<{
 		<div className="text-xs text-content-primary">
 			{hasPercent
 				? `${percentLabel} - ${formatTokenCountCompact(usedTokens)} / ${formatTokenCountCompact(contextLimitTokens)} context used`
-				: "Context usage unavailable"}
+				: hasReportedUsage
+					? "Context usage unavailable"
+					: "Context usage will appear after sending a message."}
 			{hasPercent &&
 				usage?.compressionThreshold !== undefined &&
 				usage.compressionThreshold > 0 && (
@@ -346,12 +359,7 @@ export const ContextUsageIndicator: FC<{
 					</div>
 				)}
 			{hasContextList && (
-				<div
-					className={cn(
-						"flex flex-col gap-2 text-content-secondary",
-						hasPercent && "mt-2",
-					)}
-				>
+				<div className="mt-2 flex flex-col gap-2 text-content-secondary">
 					{fileItems.length > 0 && (
 						<div className="flex flex-col gap-1">
 							<span className="font-medium text-content-primary">