diff --git a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.stories.tsx b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.stories.tsx
index 5e430d222e..3bf3b96c37 100644
--- a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.stories.tsx
+++ b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.stories.tsx
@@ -85,6 +85,8 @@ const cappedMockChats: Chat[] = Array.from(
 		diff_status: undefined,
 	}),
 );
+const longDiffURL =
+	"github.com/coder/coder/pull/26016/files/1234567890abcdef1234567890abcdef1234567890abcdef";
 
 const meta: Meta<typeof ChatSearchDialog> = {
 	title: "pages/AgentsPage/ChatSearchDialog",
@@ -123,6 +125,42 @@ type Story = StoryObj<typeof ChatSearchDialog>;
 
 export const EmptyState: Story = {};
 
+export const IconInputAlignment: Story = {
+	play: async () => {
+		const body = within(document.body);
+		const searchInput = await body.findByRole("combobox", {
+			name: "Search chats",
+		});
+		const toggleButton = await body.findByRole("button", {
+			name: "Toggle filters",
+		});
+
+		const container = toggleButton.parentElement;
+		if (!container) {
+			throw new Error("Expected the toggle button to have a parent container");
+		}
+		const searchIcon = container.querySelector("svg");
+		const filterIcon = toggleButton.querySelector("svg");
+		if (!searchIcon || !filterIcon) {
+			throw new Error("Expected the search and filter icons to render");
+		}
+
+		const verticalCenter = (element: Element) => {
+			const rect = element.getBoundingClientRect();
+			return rect.top + rect.height / 2;
+		};
+		await waitFor(() => {
+			const inputCenter = verticalCenter(searchInput);
+			expect(
+				Math.abs(verticalCenter(searchIcon) - inputCenter),
+			).toBeLessThanOrEqual(1);
+			expect(
+				Math.abs(verticalCenter(filterIcon) - inputCenter),
+			).toBeLessThanOrEqual(1);
+		});
+	},
+};
+
 export const LoadingState: Story = {
 	beforeEach: () => {
 		spyOn(API.experimental, "getChats").mockImplementation(
@@ -461,6 +499,63 @@ export const ParameterizedFilterPill: Story = {
 	},
 };
 
+export const DiffURLFilterPill: Story = {
+	beforeEach: () => {
+		spyOn(API.experimental, "getChats").mockResolvedValue(mockChats);
+	},
+	play: async () => {
+		const body = within(document.body);
+		const searchInput = body.getByRole("combobox", { name: "Search chats" });
+		const toggleButton = body.getByRole("button", { name: "Toggle filters" });
+
+		await userEvent.click(toggleButton);
+		await userEvent.click(await body.findByText("Diff URL"));
+
+		await expect(await body.findByText("diff_url:")).toBeInTheDocument();
+
+		await userEvent.click(searchInput);
+		await userEvent.type(searchInput, `${longDiffURL} `);
+
+		const diffURLPill = await body.findByText(`diff_url:${longDiffURL}`);
+		await expect(diffURLPill).toBeInTheDocument();
+		await expect(diffURLPill).toHaveAttribute(
+			"title",
+			`diff_url:${longDiffURL}`,
+		);
+		await expect(searchInput).toBeVisible();
+
+		const searchContainer = searchInput.parentElement;
+		const searchWrapper = searchContainer?.parentElement;
+		if (!searchContainer || !searchWrapper) {
+			throw new Error(
+				"Expected search input to render inside nested containers",
+			);
+		}
+
+		const dialog = searchWrapper.closest('[role="dialog"]');
+		if (!dialog) {
+			throw new Error("Expected the search input to render inside a dialog");
+		}
+
+		await waitFor(() => {
+			const dialogRight = Math.ceil(dialog.getBoundingClientRect().right);
+			expect(
+				Math.ceil(searchWrapper.getBoundingClientRect().right),
+			).toBeLessThanOrEqual(dialogRight);
+			expect(
+				Math.ceil(diffURLPill.getBoundingClientRect().right),
+			).toBeLessThanOrEqual(dialogRight);
+		});
+
+		await waitFor(() => {
+			expect(API.experimental.getChats).toHaveBeenCalledWith({
+				limit: CHAT_SEARCH_LIMIT,
+				q: `diff_url:"https://${longDiffURL}"`,
+			});
+		});
+	},
+};
+
 export const ParameterizedFilterPillEnterCommit: Story = {
 	beforeEach: () => {
 		spyOn(API.experimental, "getChats").mockResolvedValue(mockChats);
diff --git a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.tsx b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.tsx
index 25aa41dca7..963da2e9f5 100644
--- a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.tsx
+++ b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchDialog.tsx
@@ -400,7 +400,7 @@ const ChatSearchDialogContent: FC<ChatSearchDialogContentProps> = ({
 				   the dropdown, but clicks within the dropdown (which is
 				   inside the same container) don't trigger blur. */}
 			<div
-				className="relative"
+				className="relative w-full min-w-0 max-w-full"
 				onBlur={(e) => {
 					if (!e.currentTarget.contains(e.relatedTarget)) {
 						setIsDropdownOpen(false);
diff --git a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchInput.tsx b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchInput.tsx
index b134f8854b..f4722c5933 100644
--- a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchInput.tsx
+++ b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/ChatSearchInput.tsx
@@ -45,56 +45,63 @@ export const ChatSearchInput: FC<ChatSearchInputProps> = ({
 	return (
 		<div
 			className={cn(
-				"flex min-h-10 w-full items-center gap-1.5 rounded-md border border-solid border-border-default bg-surface-primary px-3",
+				"flex min-h-10 w-full min-w-0 items-start gap-1.5 rounded-md border border-solid border-border-default bg-surface-primary px-3 py-2",
 				"focus-within:ring-2 focus-within:ring-content-link",
 			)}
 		>
-			<SearchIcon className="size-4 shrink-0 text-content-secondary" />
-			{completedFilters.map((f) => (
-				<span
-					key={f.key}
-					className="inline-flex shrink-0 items-center gap-1 rounded-md border border-solid border-border bg-surface-secondary px-2 py-0.5 text-xs text-content-secondary"
-				>
-					<span>
-						{f.key}:{f.value}
-					</span>
-					<button
-						type="button"
-						onClick={(e) => {
-							e.stopPropagation();
-							onRemoveFilter(f.key);
-						}}
-						className="inline-flex cursor-pointer items-center border-none bg-transparent p-0 text-content-secondary hover:text-content-primary"
-						aria-label={`Remove ${f.key} filter`}
+			<div className="flex h-7 shrink-0 items-center">
+				<SearchIcon className="size-4 text-content-secondary" />
+			</div>
+			<div className="flex min-w-0 flex-1 flex-wrap items-center gap-1.5">
+				{completedFilters.map((f) => (
+					<span
+						key={f.key}
+						className="inline-flex max-w-full min-w-0 items-center gap-1 rounded-md border border-solid border-border bg-surface-secondary px-2 py-0.5 text-xs text-content-secondary"
 					>
-						<XIcon className="size-3" />
-					</button>
-				</span>
-			))}
-			{incompleteFilter && (
-				<span className="inline-flex shrink-0 items-center rounded-md border border-dashed border-border bg-surface-secondary px-2 py-0.5 text-xs text-content-secondary">
-					{incompleteFilter.key}:
-				</span>
-			)}
-			<input
-				ref={inputRef}
-				value={value}
-				onChange={onChange}
-				onKeyDown={onKeyDown}
-				placeholder={filters.length > 0 ? "" : "Search chats..."}
-				className="min-w-[60px] flex-1 border-none bg-transparent py-2 text-sm text-content-primary outline-none placeholder:text-content-disabled"
-				aria-label="Search chats"
-				role="combobox"
-				aria-controls={hasResults ? listboxId : undefined}
-				aria-expanded={hasResults}
-				aria-haspopup="listbox"
-				aria-activedescendant={activeResultId}
-			/>
+						<span
+							className="block min-w-0 truncate"
+							title={`${f.key}:${f.value}`}
+						>
+							{f.key}:{f.value}
+						</span>
+						<button
+							type="button"
+							onClick={(e) => {
+								e.stopPropagation();
+								onRemoveFilter(f.key);
+							}}
+							className="inline-flex shrink-0 cursor-pointer items-center border-none bg-transparent p-0 text-content-secondary hover:text-content-primary"
+							aria-label={`Remove ${f.key} filter`}
+						>
+							<XIcon className="size-3" />
+						</button>
+					</span>
+				))}
+				{incompleteFilter && (
+					<span className="inline-flex shrink-0 items-center rounded-md border border-dashed border-border bg-surface-secondary px-2 py-0.5 text-xs text-content-secondary">
+						{incompleteFilter.key}:
+					</span>
+				)}
+				<input
+					ref={inputRef}
+					value={value}
+					onChange={onChange}
+					onKeyDown={onKeyDown}
+					placeholder={filters.length > 0 ? "" : "Search chats..."}
+					className="min-w-[60px] flex-1 basis-[60px] border-none bg-transparent py-0.5 text-sm text-content-primary outline-none placeholder:text-content-disabled"
+					aria-label="Search chats"
+					role="combobox"
+					aria-controls={hasResults ? listboxId : undefined}
+					aria-expanded={hasResults}
+					aria-haspopup="listbox"
+					aria-activedescendant={activeResultId}
+				/>
+			</div>
 			<button
 				type="button"
 				onClick={onToggleDropdown}
 				className={cn(
-					"inline-flex shrink-0 cursor-pointer items-center border-none bg-transparent p-0 text-content-secondary hover:text-content-primary",
+					"inline-flex h-7 shrink-0 cursor-pointer items-center border-none bg-transparent p-0 text-content-secondary hover:text-content-primary",
 					isDropdownOpen && "text-content-primary",
 				)}
 				aria-label="Toggle filters"
diff --git a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.test.ts b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.test.ts
index 31cdaf24fa..a8121d03a0 100644
--- a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.test.ts
+++ b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.test.ts
@@ -7,7 +7,7 @@ describe("normalizeChatSearchInput", () => {
 		expect(normalizeChatSearchInput("   ")).toBeUndefined();
 	});
 
-	it("keeps key:value filters unchanged", () => {
+	it("normalizes key:value filters", () => {
 		expect(normalizeChatSearchInput("has_unread:true")).toBe("has_unread:true");
 		expect(normalizeChatSearchInput('title:"chat title" archived:true')).toBe(
 			'title:"chat title" archived:true',
@@ -20,6 +20,25 @@ describe("normalizeChatSearchInput", () => {
 				'diff_url:"https://github.com/coder/coder/pull/25391"',
 			),
 		).toBe('diff_url:"https://github.com/coder/coder/pull/25391"');
+		expect(
+			normalizeChatSearchInput(
+				"diff_url:https://github.com/coder/coder/pull/26016",
+			),
+		).toBe('diff_url:"https://github.com/coder/coder/pull/26016"');
+		expect(
+			normalizeChatSearchInput("diff_url:github.com/coder/coder/pull/26016"),
+		).toBe('diff_url:"https://github.com/coder/coder/pull/26016"');
+		expect(
+			normalizeChatSearchInput('diff_url:"github.com/coder/coder/pull/26016"'),
+		).toBe('diff_url:"https://github.com/coder/coder/pull/26016"');
+	});
+
+	it("re-quotes passthrough values containing spaces so the result round-trips", () => {
+		const normalized = normalizeChatSearchInput('pr_status:"open merged"');
+		expect(normalized).toBe('pr_status:"open merged"');
+		expect(normalizeChatSearchInput(normalized ?? "")).toBe(
+			'pr_status:"open merged"',
+		);
 	});
 
 	it("converts bare search text into a title filter", () => {
@@ -40,6 +59,11 @@ describe("normalizeChatSearchInput", () => {
 		expect(normalizeChatSearchInput("fix has_unread:true auth")).toBe(
 			'has_unread:true title:"fix auth"',
 		);
+		expect(
+			normalizeChatSearchInput(
+				"diff_url:https://github.com/coder/coder/pull/26016 fix",
+			),
+		).toBe('diff_url:"https://github.com/coder/coder/pull/26016" title:"fix"');
 		expect(
 			normalizeChatSearchInput('archived:true title:"chat title" fix'),
 		).toBe('archived:true title:"chat title fix"');
diff --git a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.ts b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.ts
index 1b26b6770e..349593f528 100644
--- a/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.ts
+++ b/site/src/pages/AgentsPage/components/ChatsSidebar/dialogs/searchQuery.ts
@@ -6,6 +6,10 @@ const sanitizeChatSearchValue = (value: string): string => {
 	return value.replaceAll('"', "");
 };
 
+const addDefaultURLScheme = (value: string): string => {
+	return /^[a-z][a-z\d+\-.]*:\/\//i.test(value) ? value : `https://${value}`;
+};
+
 // Filter keys that may pass through to the backend unchanged. `title` is not
 // listed here because bare text and `title:` filters are merged into a single
 // title filter; see the title-handling branch in normalizeChatSearchInput.
@@ -62,7 +66,7 @@ const getKeyValueDelimiterIndex = (token: string): number | undefined => {
 
 const getKeyValuePair = (
 	token: string,
-): { key: string; value: string } | undefined => {
+): { key: string; rawKey: string; value: string } | undefined => {
 	const delimiterIndex = getKeyValueDelimiterIndex(token);
 	if (
 		delimiterIndex === undefined ||
@@ -72,18 +76,40 @@ const getKeyValuePair = (
 		return undefined;
 	}
 
+	const rawKey = token.slice(0, delimiterIndex).replaceAll('"', "");
 	return {
-		key: token.slice(0, delimiterIndex).replaceAll('"', "").toLowerCase(),
+		key: rawKey.toLowerCase(),
+		rawKey,
 		value: token.slice(delimiterIndex + 1).replace(/^"|"$/g, ""),
 	};
 };
 
+// The backend splits on unquoted whitespace and colons, so values containing
+// either (e.g. a diff URL) must be quoted.
+const normalizePassthroughChatSearchFilter = ({
+	key,
+	rawKey,
+	value,
+}: {
+	readonly key: string;
+	readonly rawKey: string;
+	readonly value: string;
+}): string => {
+	const sanitizedValue =
+		key === "diff_url"
+			? addDefaultURLScheme(sanitizeChatSearchValue(value))
+			: sanitizeChatSearchValue(value);
+	return sanitizedValue.includes(":") || sanitizedValue.includes(" ")
+		? `${rawKey}:"${sanitizedValue}"`
+		: `${rawKey}:${sanitizedValue}`;
+};
+
 /**
  * Normalizes raw search input into a query string the chat search API accepts.
  *
  * Bare text and `title:` filters are merged into a single `title:"..."`
  * filter (the backend rejects a parameter that appears more than once).
- * Recognized `key:value` filters pass through unchanged.
+ * Recognized `key:value` filters are normalized for backend syntax.
  */
 export const normalizeChatSearchInput = (
 	rawInput: string,
@@ -94,7 +120,8 @@ export const normalizeChatSearchInput = (
 	}
 
 	const tokens = splitSearchInput(trimmedInput);
-	const keyValuePairs: string[] = [];
+	const passthroughFilters: string[] = [];
+	const normalizedTokens: string[] = [];
 	const titleTerms: string[] = [];
 	let hasBareTitleText = false;
 
@@ -107,6 +134,7 @@ export const normalizeChatSearchInput = (
 		}
 
 		if (keyValuePair.key === "title") {
+			normalizedTokens.push(token);
 			titleTerms.push(keyValuePair.value);
 			continue;
 		}
@@ -117,7 +145,9 @@ export const normalizeChatSearchInput = (
 			continue;
 		}
 
-		keyValuePairs.push(token);
+		const normalizedFilter = normalizePassthroughChatSearchFilter(keyValuePair);
+		passthroughFilters.push(normalizedFilter);
+		normalizedTokens.push(normalizedFilter);
 	}
 
 	// Multiple title values must be merged into a single title filter because
@@ -127,11 +157,11 @@ export const normalizeChatSearchInput = (
 	}
 
 	if (!hasBareTitleText) {
-		return trimmedInput;
+		return normalizedTokens.join(" ");
 	}
 
 	return [
-		...keyValuePairs,
+		...passthroughFilters,
 		`title:"${sanitizeChatSearchValue(titleTerms.join(" "))}"`,
 	].join(" ");
 };