diff --git a/site/src/pages/AISettingsPage/ModelsPage/components/ModelForm.stories.tsx b/site/src/pages/AISettingsPage/ModelsPage/components/ModelForm.stories.tsx
index 7c1c3bf54cac5..d7eeea19fbc6a 100644
--- a/site/src/pages/AISettingsPage/ModelsPage/components/ModelForm.stories.tsx
+++ b/site/src/pages/AISettingsPage/ModelsPage/components/ModelForm.stories.tsx
@@ -1,9 +1,22 @@
 import type { Meta, StoryObj } from "@storybook/react-vite";
-import { expect, fn, screen, spyOn, userEvent, within } from "storybook/test";
+import {
+	expect,
+	fn,
+	mocked,
+	screen,
+	spyOn,
+	userEvent,
+	waitFor,
+	within,
+} from "storybook/test";
 import { reactRouterParameters } from "storybook-addon-remix-react-router";
 import { API } from "#/api/api";
 import { aiModelPrices } from "#/api/queries/aiProviders";
 import type * as TypesGen from "#/api/typesGenerated";
+import {
+	MockGPT5BelowThresholdModelPrice,
+	MockGPT5ModelPrice,
+} from "#/testHelpers/chatModels";
 import { withDashboardProvider, withToaster } from "#/testHelpers/storybook";
 import {
 	MockAnthropicProviderState,
@@ -23,6 +36,15 @@ const onUpdateModel = fn(
 	): Promise<unknown> => undefined,
 );
 
+// The price loading placeholder is transient: it disappears once the
+// debounce settles and the lookup resolves, so poll for it instead of
+// asserting synchronously.
+const waitForPriceLoading = async (canvas: ReturnType<typeof within>) => {
+	await waitFor(() =>
+		expect(canvas.getByLabelText("Input price loading")).toBeInTheDocument(),
+	);
+};
+
 const meta: Meta<typeof ModelForm> = {
 	title: "pages/AISettingsPage/ModelsPage/ModelForm",
 	component: ModelForm,
@@ -484,18 +506,7 @@ export const CostEstimateFromLivePriceBook: Story = {
 		queries: [
 			{
 				key: aiModelPrices("openai", "gpt-5").queryKey,
-				data: [
-					{
-						provider: "openai",
-						model: "gpt-5",
-						input_price: 1250000,
-						output_price: 10000000,
-						cache_read_price: 125000,
-						cache_write_price: null,
-						created_at: "2026-02-18T12:00:00.000Z",
-						updated_at: "2026-02-18T12:00:00.000Z",
-					},
-				],
+				data: [MockGPT5ModelPrice],
 			},
 		],
 	},
@@ -511,6 +522,123 @@ export const CostEstimateFromLivePriceBook: Story = {
 	},
 };
 
+// A live price below $0.0001 per million tokens would render as $0.00 and
+// read as free, so the field shows a threshold instead.
+export const CostEstimateBelowThresholdPrice: Story = {
+	args: {
+		editingModel: mockGPT5,
+		onDeleteModel: fn(async () => undefined),
+	},
+	parameters: {
+		queries: [
+			{
+				key: aiModelPrices("openai", "gpt-5").queryKey,
+				data: [MockGPT5BelowThresholdModelPrice],
+			},
+		],
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		const inputField = canvas.getByLabelText(/^input$/i);
+		await expect(inputField).toHaveValue("0.0001");
+		await expect(canvas.getByText("<$")).toBeInTheDocument();
+		// The threshold marker is part of the input's accessible description
+		// so screen readers announce "less than $0.0001" rather than an exact
+		// price.
+		await expect(inputField).toHaveAccessibleDescription(
+			"less than $0.0001 USD per million tokens",
+		);
+	},
+};
+
+// Editing the model identifier fires a live price lookup per settled value
+// rather than per keystroke, so typing a full identifier costs one request.
+export const CostEstimateDebouncesLivePriceLookup: Story = {
+	args: {
+		editingModel: mockGPT5,
+		onDeleteModel: fn(async () => undefined),
+	},
+	beforeEach: () => {
+		spyOn(API.experimental, "getAIModelPrices").mockResolvedValue([]);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		const modelInput = canvas.getByLabelText(/model identifier/i);
+		await userEvent.clear(modelInput);
+		await userEvent.type(modelInput, "gpt-5.5");
+		await waitFor(() =>
+			expect(API.experimental.getAIModelPrices).toHaveBeenCalledWith({
+				provider: "openai",
+				model: "gpt-5.5",
+			}),
+		);
+		const calls = mocked(API.experimental.getAIModelPrices).mock.calls.map(
+			([params]) => params.model,
+		);
+		expect(calls).toStrictEqual(["gpt-5", "gpt-5.5"]);
+	},
+};
+
+// On an entitled form the live lookup may override the catalog, so typing
+// into an empty identifier shows the loading placeholder immediately rather
+// than briefly flashing catalog prices before the lookup fires.
+export const CostEstimateShowsLoadingWhileDebouncePending: Story = {
+	args: {
+		selectedProviderState: MockAnthropicProviderState,
+	},
+	beforeEach: () => {
+		spyOn(API.experimental, "getAIModelPrices").mockResolvedValue([]);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		await userEvent.type(
+			canvas.getByLabelText(/model identifier/i),
+			"claude-haiku-4-5",
+		);
+		await waitForPriceLoading(canvas);
+		// The catalog price must not render while the lookup is pending.
+		expect(canvas.queryByDisplayValue("1")).not.toBeInTheDocument();
+	},
+};
+
+// Clearing the identifier discards the settled live price immediately:
+// until the debounce settles the section shows the loading placeholder
+// rather than the previous model's prices.
+export const CostEstimateClearingModelDiscardsStalePrices: Story = {
+	args: {
+		editingModel: mockGPT5,
+		onDeleteModel: fn(async () => undefined),
+	},
+	parameters: {
+		queries: [
+			{
+				key: aiModelPrices("openai", "gpt-5").queryKey,
+				data: [MockGPT5ModelPrice],
+			},
+		],
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		await expect(canvas.getByLabelText(/^input$/i)).toHaveValue("1.25");
+
+		await userEvent.clear(canvas.getByLabelText(/model identifier/i));
+		await waitForPriceLoading(canvas);
+		expect(canvas.queryByDisplayValue("1.25")).not.toBeInTheDocument();
+	},
+};
+
 // A price book row is the deployment's own pricing, so it wins outright. A
 // null category on the row means the model is unpriced there and bills as
 // zero, so the field stays blank instead of falling back to the catalog.
@@ -602,6 +730,63 @@ export const CostEstimateCatalogOnlyWhenNotEntitled: Story = {
 	},
 };
 
+// Without the entitlement the live price query is disabled, so changing the
+// model identifier must not flash loading placeholders: catalog prices are
+// synchronously available and update immediately.
+export const CostEstimateCatalogNotHiddenByDebounce: Story = {
+	args: {
+		editingModel: mockClaude,
+		selectedProviderState: MockAnthropicProviderState,
+		onDeleteModel: fn(async () => undefined),
+	},
+	parameters: {
+		features: [],
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		const modelInput = canvas.getByLabelText(/model identifier/i);
+		await userEvent.clear(modelInput);
+		await userEvent.type(modelInput, "claude-haiku-4-5");
+		await expect(canvas.getByLabelText(/^input$/i)).toHaveValue("1");
+		expect(canvas.queryByLabelText(/price loading/i)).not.toBeInTheDocument();
+	},
+};
+
+// A failed lookup must not linger while the debounce settles for a new
+// model: the section shows the loading placeholder until the new request
+// has actually fired.
+export const CostEstimateErrorClearsWhileDebouncePending: Story = {
+	args: {
+		editingModel: mockClaude,
+		selectedProviderState: MockAnthropicProviderState,
+		onDeleteModel: fn(async () => undefined),
+	},
+	beforeEach: () => {
+		spyOn(API.experimental, "getAIModelPrices").mockRejectedValue(
+			new Error("request failed"),
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /cost estimate/i }),
+		);
+		await expect(
+			canvas.getByText("Couldn't load pricing."),
+		).toBeInTheDocument();
+
+		const modelInput = canvas.getByLabelText(/model identifier/i);
+		await userEvent.type(modelInput, "-20251001");
+		await waitForPriceLoading(canvas);
+		expect(
+			canvas.queryByText("Couldn't load pricing."),
+		).not.toBeInTheDocument();
+	},
+};
+
 // While the price book lookup is in flight, the four boxes stay rendered
 // with a loading placeholder in each instead of a catalog price. The
 // catalog must not appear because the model may have a deployment override.
diff --git a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/ModelConfigFields.tsx b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/ModelConfigFields.tsx
index d0456815f2c7a..5a537951e684e 100644
--- a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/ModelConfigFields.tsx
+++ b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/ModelConfigFields.tsx
@@ -32,6 +32,7 @@ import {
 	TooltipContent,
 	TooltipTrigger,
 } from "#/components/Tooltip/Tooltip";
+import { useDebouncedValue } from "#/hooks/debounce";
 import { normalizeProvider } from "#/modules/aiModels/helpers";
 import { useFeatureVisibility } from "#/modules/dashboard/useFeatureVisibility";
 import { cn } from "#/utils/cn";
@@ -683,14 +684,25 @@ export const PricingEstimateFields: FC<{
 	const aibridgeEntitled = Boolean(useFeatureVisibility().aibridge);
 	const normalizedProvider = normalizeProvider(provider);
 	const trimmedModel = model.trim();
+	// Debounce the pair so the lookup never mixes a new provider with the
+	// previous model identifier.
+	const debouncedLookup = useDebouncedValue(
+		{ provider: normalizedProvider, model: trimmedModel },
+		500,
+	);
+	const entitledWithProvider = aibridgeEntitled && normalizedProvider !== "";
 	const livePricesQuery = useQuery({
-		...aiModelPrices(normalizedProvider, trimmedModel),
-		enabled:
-			aibridgeEntitled && normalizedProvider !== "" && trimmedModel !== "",
+		...aiModelPrices(debouncedLookup.provider, debouncedLookup.model),
+		enabled: entitledWithProvider && debouncedLookup.model !== "",
 	});
+	const debouncePending =
+		entitledWithProvider &&
+		(debouncedLookup.provider !== normalizedProvider ||
+			debouncedLookup.model !== trimmedModel);
 	const livePriceLoading =
-		livePricesQuery.fetchStatus !== "idle" && !livePricesQuery.isSuccess;
-	const livePrice = livePricesQuery.data?.[0];
+		debouncePending ||
+		(livePricesQuery.fetchStatus !== "idle" && !livePricesQuery.isSuccess);
+	const livePrice = debouncePending ? undefined : livePricesQuery.data?.[0];
 
 	const knownModel =
 		findKnownModelByCanonicalId(normalizedProvider, trimmedModel) ??
@@ -709,7 +721,7 @@ export const PricingEstimateFields: FC<{
 			}
 		: knownModel;
 
-	if (livePricesQuery.isError) {
+	if (!debouncePending && livePricesQuery.isError) {
 		return (
 			<p className="m-0 flex items-center gap-1.5 text-xs text-content-secondary sm:col-span-full">
 				<InfoIcon className="size-3.5 shrink-0" />
@@ -735,13 +747,15 @@ export const PricingEstimateFields: FC<{
 			{priceEstimateFields.map(([label, key]) => {
 				const cost = costs?.[key];
 				const fieldId = `${fieldIdPrefix}-${label.toLowerCase().replace(/\s+/g, "-")}`;
-				const displayValue =
-					cost === undefined ? "" : formatPricePerMillionTokens(cost).slice(1);
+				const price =
+					cost === undefined ? undefined : formatPricePerMillionTokens(cost);
 				return (
 					<div key={label} className="flex min-w-0 flex-col gap-1.5">
 						<FieldLabel htmlFor={fieldId} label={label} />
 						<InputGroup className="cursor-not-allowed bg-surface-secondary">
-							<InputGroupAddon align="inline-start">$</InputGroupAddon>
+							<InputGroupAddon align="inline-start">
+								{price?.belowThreshold ? "<$" : "$"}
+							</InputGroupAddon>
 							{livePriceLoading ? (
 								<Skeleton
 									aria-label={`${label} price loading`}
@@ -751,10 +765,18 @@ export const PricingEstimateFields: FC<{
 								<InputGroupInput
 									id={fieldId}
 									className="min-w-0 cursor-not-allowed text-content-secondary"
-									value={displayValue}
+									value={price?.value ?? ""}
+									aria-describedby={
+										price?.belowThreshold ? `${fieldId}-threshold` : undefined
+									}
 									readOnly
 								/>
 							)}
+							{price?.belowThreshold && !livePriceLoading && (
+								<span id={`${fieldId}-threshold`} className="sr-only">
+									{`less than $${price.value} USD per million tokens`}
+								</span>
+							)}
 							<InputGroupAddon align="inline-end">
 								<span className="text-xs text-content-disabled">
 									USD/1M tokens
diff --git a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.test.ts b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.test.ts
index b49c3567322b1..b45f9c7d7cacc 100644
--- a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.test.ts
+++ b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.test.ts
@@ -126,29 +126,38 @@ describe("findKnownModelByExactAlias", () => {
 
 describe("formatPricePerMillionTokens", () => {
 	it("formats whole-dollar prices", () => {
-		expect(formatPricePerMillionTokens(10)).toBe("$10");
+		expect(formatPricePerMillionTokens(10)).toStrictEqual({
+			belowThreshold: false,
+			value: "10",
+		});
 	});
 
 	it("formats fractional prices without dropping precision", () => {
-		expect(formatPricePerMillionTokens(1.25)).toBe("$1.25");
-		expect(formatPricePerMillionTokens(0.1)).toBe("$0.10");
-		expect(formatPricePerMillionTokens(0.3)).toBe("$0.30");
+		expect(formatPricePerMillionTokens(1.25).value).toBe("1.25");
+		expect(formatPricePerMillionTokens(0.1).value).toBe("0.10");
+		expect(formatPricePerMillionTokens(0.3).value).toBe("0.30");
 	});
 
 	it("keeps sub-cent prices visible", () => {
-		expect(formatPricePerMillionTokens(0.075)).toBe("$0.075");
-		expect(formatPricePerMillionTokens(0.003625)).toBe("$0.0036");
-		expect(formatPricePerMillionTokens(0.125)).toBe("$0.125");
+		expect(formatPricePerMillionTokens(0.075).value).toBe("0.075");
+		expect(formatPricePerMillionTokens(0.003625).value).toBe("0.0036");
+		expect(formatPricePerMillionTokens(0.125).value).toBe("0.125");
 	});
 
-	it("shows a threshold for positive prices below four decimals", () => {
-		expect(formatPricePerMillionTokens(0.000001)).toBe("<$0.0001");
-		expect(formatPricePerMillionTokens(0.000049)).toBe("<$0.0001");
-		expect(formatPricePerMillionTokens(0.0001)).toBe("$0.0001");
+	it("flags positive prices below four decimals as a threshold", () => {
+		expect(formatPricePerMillionTokens(0.000001)).toStrictEqual({
+			belowThreshold: true,
+			value: "0.0001",
+		});
+		expect(formatPricePerMillionTokens(0.000049).belowThreshold).toBe(true);
+		expect(formatPricePerMillionTokens(0.0001)).toStrictEqual({
+			belowThreshold: false,
+			value: "0.0001",
+		});
 	});
 
 	it("formats zero", () => {
-		expect(formatPricePerMillionTokens(0)).toBe("$0");
+		expect(formatPricePerMillionTokens(0).value).toBe("0");
 	});
 
 	it("rejects non-finite values", () => {
diff --git a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.ts b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.ts
index 765face1b66e4..1e918138e3306 100644
--- a/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.ts
+++ b/site/src/pages/AgentsPage/components/ChatModelAdminPanel/knownModels/index.ts
@@ -101,21 +101,23 @@ export const formatContextBadge = (contextLimit: number): string => {
 	return `${formatCompactNumber(contextLimit / 1_000_000)}M context`;
 };
 
-export const formatPricePerMillionTokens = (value: number): string => {
+export const formatPricePerMillionTokens = (
+	value: number,
+): { belowThreshold: boolean; value: string } => {
 	if (!Number.isFinite(value)) {
 		throw new Error("price must be a finite number");
 	}
 	if (Number.isInteger(value)) {
-		return `$${value}`;
+		return { belowThreshold: false, value: String(value) };
 	}
 	// A positive price too small to show at four decimals would otherwise
 	// render as $0.00 and read as free, so show it as a threshold instead.
 	if (value > 0 && value < 0.0001) {
-		return "<$0.0001";
+		return { belowThreshold: true, value: "0.0001" };
 	}
-	// Keep two decimals so cents read as cents ($0.10, not $0.1). Keep up to
-	// four so sub-cent prices stay visible ($0.075, $0.0036).
+	// Keep two decimals so cents read as cents (0.10, not 0.1). Keep up to
+	// four so sub-cent prices stay visible (0.075, 0.0036).
 	const [whole, decimals = ""] = value.toFixed(4).split(".");
 	const trimmed = decimals.slice(0, 2) + decimals.slice(2).replace(/0+$/, "");
-	return `$${whole}.${trimmed}`;
+	return { belowThreshold: false, value: `${whole}.${trimmed}` };
 };
diff --git a/site/src/testHelpers/chatModels.ts b/site/src/testHelpers/chatModels.ts
index 0a3c021fd9bad..e1ad922911267 100644
--- a/site/src/testHelpers/chatModels.ts
+++ b/site/src/testHelpers/chatModels.ts
@@ -1,4 +1,5 @@
 import type {
+	AIModelPrice,
 	ChatModelConfig,
 	ChatModelProvider,
 	ChatProviderConfig,
@@ -39,3 +40,24 @@ export const MockChatModelProvider: ChatModelProvider = {
 	available: true,
 	models: [],
 };
+
+// Prices are micro-units per million tokens.
+export const MockGPT5ModelPrice: AIModelPrice = {
+	provider: "openai",
+	model: "gpt-5",
+	input_price: 1250000,
+	output_price: 10000000,
+	cache_read_price: 125000,
+	cache_write_price: null,
+	created_at: MOCK_TIMESTAMP,
+	updated_at: MOCK_TIMESTAMP,
+};
+
+// An input price below $0.0001 per million tokens renders as a threshold
+// rather than an exact value.
+export const MockGPT5BelowThresholdModelPrice: AIModelPrice = {
+	...MockGPT5ModelPrice,
+	input_price: 50,
+	output_price: null,
+	cache_read_price: null,
+};