diff --git a/site/src/components/Autocomplete/Autocomplete.stories.tsx b/site/src/components/Autocomplete/Autocomplete.stories.tsx
new file mode 100644
index 0000000000000..9639e8a89b454
--- /dev/null
+++ b/site/src/components/Autocomplete/Autocomplete.stories.tsx
@@ -0,0 +1,354 @@
+import type { Meta, StoryObj } from "@storybook/react-vite";
+import { Avatar } from "components/Avatar/Avatar";
+import { AvatarData } from "components/Avatar/AvatarData";
+import { Check } from "lucide-react";
+import { useState } from "react";
+import { expect, screen, userEvent, waitFor, within } from "storybook/test";
+import { Autocomplete } from "./Autocomplete";
+
+const meta: Meta<typeof Autocomplete> = {
+	title: "components/Autocomplete",
+	component: Autocomplete,
+	args: {
+		placeholder: "Select an option",
+	},
+};
+
+export default meta;
+
+type Story = StoryObj<typeof Autocomplete>;
+
+interface SimpleOption {
+	id: string;
+	name: string;
+}
+
+const simpleOptions: SimpleOption[] = [
+	{ id: "1", name: "Mango" },
+	{ id: "2", name: "Banana" },
+	{ id: "3", name: "Pineapple" },
+	{ id: "4", name: "Kiwi" },
+	{ id: "5", name: "Coconut" },
+];
+
+export const Default: Story = {
+	render: function DefaultStory() {
+		const [value, setValue] = useState<SimpleOption | null>(null);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		const trigger = canvas.getByRole("button");
+
+		expect(trigger).toHaveTextContent("Select a fruit");
+		await userEvent.click(trigger);
+
+		await waitFor(() =>
+			expect(screen.getByRole("option", { name: "Mango" })).toBeInTheDocument(),
+		);
+	},
+};
+
+export const WithSelectedValue: Story = {
+	render: function WithSelectedValueStory() {
+		const [value, setValue] = useState<SimpleOption | null>(simpleOptions[2]);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		const trigger = canvas.getByRole("button", { name: /pineapple/i });
+		expect(trigger).toHaveTextContent("Pineapple");
+
+		await userEvent.click(trigger);
+
+		await waitFor(() =>
+			expect(
+				screen.getByRole("option", { name: "Pineapple" }),
+			).toBeInTheDocument(),
+		);
+
+		await userEvent.click(screen.getByRole("option", { name: "Mango" }));
+		await waitFor(() => expect(trigger).toHaveTextContent("Mango"));
+	},
+};
+
+export const NotClearable: Story = {
+	render: function NotClearableStory() {
+		const [value, setValue] = useState<SimpleOption | null>(simpleOptions[0]);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+					clearable={false}
+				/>
+			</div>
+		);
+	},
+};
+
+export const Loading: Story = {
+	render: function LoadingStory() {
+		const [value, setValue] = useState<SimpleOption | null>(null);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={[]}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Loading options..."
+					loading
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(canvas.getByRole("button"));
+		await waitFor(() => {
+			const spinners = screen.getAllByTitle("Loading spinner");
+			expect(spinners.length).toBeGreaterThanOrEqual(1);
+		});
+	},
+};
+
+export const Disabled: Story = {
+	render: function DisabledStory() {
+		const [value, setValue] = useState<SimpleOption | null>(simpleOptions[1]);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+					disabled
+				/>
+			</div>
+		);
+	},
+};
+
+export const EmptyOptions: Story = {
+	render: function EmptyOptionsStory() {
+		const [value, setValue] = useState<SimpleOption | null>(null);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={[]}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+					noOptionsText="No fruits available"
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(canvas.getByRole("button"));
+		await waitFor(() =>
+			expect(screen.getByText("No fruits available")).toBeInTheDocument(),
+		);
+	},
+};
+
+export const SearchAndFilter: Story = {
+	render: function SearchAndFilterStory() {
+		const [value, setValue] = useState<SimpleOption | null>(null);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		await userEvent.click(
+			canvas.getByRole("button", { name: /select a fruit/i }),
+		);
+		const searchInput = screen.getByRole("combobox");
+		await userEvent.type(searchInput, "an");
+
+		await waitFor(() => {
+			expect(screen.getByRole("option", { name: "Mango" })).toBeInTheDocument();
+			expect(
+				screen.getByRole("option", { name: "Banana" }),
+			).toBeInTheDocument();
+			expect(
+				screen.queryByRole("option", { name: "Pineapple" }),
+			).not.toBeInTheDocument();
+		});
+	},
+};
+
+export const ClearSelection: Story = {
+	render: function ClearSelectionStory() {
+		const [value, setValue] = useState<SimpleOption | null>(simpleOptions[0]);
+		return (
+			<div className="w-80">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={simpleOptions}
+					getOptionValue={(opt) => opt.id}
+					getOptionLabel={(opt) => opt.name}
+					placeholder="Select a fruit"
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		const trigger = canvas.getByRole("button", { name: /mango/i });
+		expect(trigger).toHaveTextContent("Mango");
+
+		const clearButton = canvas.getByRole("button", { name: "Clear selection" });
+		await userEvent.click(clearButton);
+
+		await waitFor(() =>
+			expect(
+				canvas.getByRole("button", { name: /select a fruit/i }),
+			).toBeInTheDocument(),
+		);
+	},
+};
+
+interface User {
+	id: string;
+	username: string;
+	email: string;
+	avatar_url?: string;
+}
+
+const users: User[] = [
+	{
+		id: "1",
+		username: "alice",
+		email: "alice@example.com",
+		avatar_url: "",
+	},
+	{
+		id: "2",
+		username: "bob",
+		email: "bob@example.com",
+		avatar_url: "",
+	},
+	{
+		id: "3",
+		username: "charlie",
+		email: "charlie@example.com",
+		avatar_url: "",
+	},
+];
+
+export const WithCustomRenderOption: Story = {
+	render: function WithCustomRenderOptionStory() {
+		const [value, setValue] = useState<User | null>(null);
+		return (
+			<div className="w-[350px]">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={users}
+					getOptionValue={(user) => user.id}
+					getOptionLabel={(user) => user.email}
+					placeholder="Search for a user"
+					renderOption={(user, isSelected) => (
+						<div className="flex items-center justify-between w-full">
+							<AvatarData
+								title={user.username}
+								subtitle={user.email}
+								src={user.avatar_url}
+							/>
+							{isSelected && <Check className="size-4 shrink-0" />}
+						</div>
+					)}
+				/>
+			</div>
+		);
+	},
+	play: async ({ canvasElement }) => {
+		const canvas = within(canvasElement);
+		const trigger = canvas.getByRole("button");
+
+		expect(trigger).toHaveTextContent("Search for a user");
+		await userEvent.click(trigger);
+	},
+};
+
+export const WithStartAdornment: Story = {
+	render: function WithStartAdornmentStory() {
+		const [value, setValue] = useState<User | null>(users[0]);
+		return (
+			<div className="w-[350px]">
+				<Autocomplete
+					value={value}
+					onChange={setValue}
+					options={users}
+					getOptionValue={(user) => user.id}
+					getOptionLabel={(user) => user.email}
+					placeholder="Search for a user"
+					startAdornment={
+						value && (
+							<Avatar
+								size="sm"
+								src={value.avatar_url}
+								fallback={value.username}
+							/>
+						)
+					}
+					renderOption={(user, isSelected) => (
+						<div className="flex items-center justify-between w-full">
+							<AvatarData
+								title={user.username}
+								subtitle={user.email}
+								src={user.avatar_url}
+							/>
+							{isSelected && <Check className="size-4 shrink-0" />}
+						</div>
+					)}
+				/>
+			</div>
+		);
+	},
+};
diff --git a/site/src/components/Autocomplete/Autocomplete.tsx b/site/src/components/Autocomplete/Autocomplete.tsx
new file mode 100644
index 0000000000000..5872927420569
--- /dev/null
+++ b/site/src/components/Autocomplete/Autocomplete.tsx
@@ -0,0 +1,252 @@
+import {
+	Command,
+	CommandEmpty,
+	CommandGroup,
+	CommandInput,
+	CommandItem,
+	CommandList,
+} from "components/Command/Command";
+import {
+	Popover,
+	PopoverContent,
+	PopoverTrigger,
+} from "components/Popover/Popover";
+import { Spinner } from "components/Spinner/Spinner";
+import { Check, ChevronDown, X } from "lucide-react";
+import {
+	type KeyboardEvent,
+	type ReactNode,
+	useCallback,
+	useState,
+} from "react";
+import { cn } from "utils/cn";
+
+interface AutocompleteProps<TOption> {
+	value: TOption | null;
+	onChange: (value: TOption | null) => void;
+	options: readonly TOption[];
+	getOptionValue: (option: TOption) => string;
+	getOptionLabel: (option: TOption) => string;
+	isOptionEqualToValue?: (option: TOption, value: TOption) => boolean;
+	renderOption?: (option: TOption, isSelected: boolean) => ReactNode;
+	loading?: boolean;
+	placeholder?: string;
+	noOptionsText?: string;
+	open?: boolean;
+	onOpenChange?: (open: boolean) => void;
+	inputValue?: string;
+	onInputChange?: (value: string) => void;
+	clearable?: boolean;
+	disabled?: boolean;
+	startAdornment?: ReactNode;
+	className?: string;
+	id?: string;
+	"data-testid"?: string;
+}
+
+export function Autocomplete<TOption>({
+	value,
+	onChange,
+	options,
+	getOptionValue,
+	getOptionLabel,
+	isOptionEqualToValue,
+	renderOption,
+	loading = false,
+	placeholder = "Select an option",
+	noOptionsText = "No results found",
+	open: controlledOpen,
+	onOpenChange,
+	inputValue: controlledInputValue,
+	onInputChange,
+	clearable = true,
+	disabled = false,
+	startAdornment,
+	className,
+	id,
+	"data-testid": testId,
+}: AutocompleteProps<TOption>) {
+	const [managedOpen, setManagedOpen] = useState(false);
+	const [managedInputValue, setManagedInputValue] = useState("");
+
+	const isOpen = controlledOpen ?? managedOpen;
+	const inputValue = controlledInputValue ?? managedInputValue;
+
+	const handleOpenChange = useCallback(
+		(newOpen: boolean) => {
+			setManagedOpen(newOpen);
+			onOpenChange?.(newOpen);
+			if (!newOpen && controlledInputValue === undefined) {
+				setManagedInputValue("");
+			}
+		},
+		[onOpenChange, controlledInputValue],
+	);
+
+	const handleInputChange = useCallback(
+		(newValue: string) => {
+			setManagedInputValue(newValue);
+			onInputChange?.(newValue);
+		},
+		[onInputChange],
+	);
+
+	const isSelected = useCallback(
+		(option: TOption): boolean => {
+			if (!value) return false;
+			if (isOptionEqualToValue) {
+				return isOptionEqualToValue(option, value);
+			}
+			return getOptionValue(option) === getOptionValue(value);
+		},
+		[value, isOptionEqualToValue, getOptionValue],
+	);
+
+	const handleSelect = useCallback(
+		(option: TOption) => {
+			if (isSelected(option) && clearable) {
+				onChange(null);
+			} else {
+				onChange(option);
+			}
+			handleOpenChange(false);
+		},
+		[isSelected, clearable, onChange, handleOpenChange],
+	);
+
+	const handleClear = useCallback(
+		(e: React.SyntheticEvent) => {
+			e.stopPropagation();
+			onChange(null);
+			handleInputChange("");
+		},
+		[onChange, handleInputChange],
+	);
+
+	const handleKeyDown = useCallback(
+		(e: KeyboardEvent<HTMLInputElement>) => {
+			if (e.key === "Escape") {
+				handleOpenChange(false);
+			}
+		},
+		[handleOpenChange],
+	);
+
+	const displayValue = value ? getOptionLabel(value) : "";
+	const showClearButton = clearable && value && !disabled;
+
+	return (
+		<Popover open={isOpen} onOpenChange={handleOpenChange}>
+			<PopoverTrigger asChild disabled={disabled}>
+				<button
+					type="button"
+					id={id}
+					data-testid={testId}
+					aria-expanded={isOpen}
+					aria-haspopup="listbox"
+					disabled={disabled}
+					className={cn(
+						`flex h-10 w-full items-center justify-between gap-2
+						rounded-md border border-border border-solid bg-transparent px-3 py-2
+						text-sm shadow-sm transition-colors
+						placeholder:text-content-secondary
+						focus-visible:outline-none focus-visible:ring-2 focus-visible:ring-content-link
+						disabled:cursor-not-allowed disabled:opacity-50`,
+						className,
+					)}
+				>
+					<span className="flex items-center gap-2 overflow-hidden flex-1 min-w-0">
+						{startAdornment}
+						<span
+							className={cn(
+								"truncate text-left",
+								displayValue
+									? "text-content-primary"
+									: "text-content-secondary",
+							)}
+						>
+							{displayValue || placeholder}
+						</span>
+					</span>
+					<span className="flex items-center shrink-0">
+						{loading && <Spinner size="sm" loading className="mr-1" />}
+						{showClearButton && (
+							<span
+								role="button"
+								tabIndex={0}
+								onClick={handleClear}
+								onKeyDown={(e) => {
+									if (e.key === "Enter" || e.key === " ") {
+										handleClear(e);
+									}
+								}}
+								className="flex items-center justify-center size-5 rounded hover:bg-surface-secondary transition-colors"
+								aria-label="Clear selection"
+							>
+								<X className="size-4 text-content-secondary hover:text-content-primary" />
+							</span>
+						)}
+						<span className="flex items-center justify-center size-5">
+							<ChevronDown
+								className={cn(
+									"size-4 text-content-secondary transition-transform",
+									isOpen && "rotate-180",
+								)}
+							/>
+						</span>
+					</span>
+				</button>
+			</PopoverTrigger>
+			<PopoverContent
+				className="w-[var(--radix-popover-trigger-width)] p-0"
+				align="start"
+			>
+				<Command shouldFilter={controlledInputValue === undefined}>
+					<CommandInput
+						placeholder={placeholder}
+						value={inputValue}
+						onValueChange={handleInputChange}
+						onKeyDown={handleKeyDown}
+					/>
+					<CommandList>
+						{loading ? (
+							<div className="flex items-center justify-center py-6">
+								<Spinner size="sm" loading />
+							</div>
+						) : (
+							<>
+								<CommandEmpty>{noOptionsText}</CommandEmpty>
+								<CommandGroup>
+									{options.map((option) => {
+										const optionValue = getOptionValue(option);
+										const optionLabel = getOptionLabel(option);
+										const selected = isSelected(option);
+
+										return (
+											<CommandItem
+												key={optionValue}
+												value={optionValue}
+												keywords={[optionLabel]}
+												onSelect={() => handleSelect(option)}
+												className="cursor-pointer"
+											>
+												{renderOption ? (
+													renderOption(option, selected)
+												) : (
+													<>
+														<span className="flex-1">{optionLabel}</span>
+														{selected && <Check className="size-4 shrink-0" />}
+													</>
+												)}
+											</CommandItem>
+										);
+									})}
+								</CommandGroup>
+							</>
+						)}
+					</CommandList>
+				</Command>
+			</PopoverContent>
+		</Popover>
+	);
+}
diff --git a/site/src/components/UserOrGroupAutocomplete/UserOrGroupOption.tsx b/site/src/components/UserOrGroupAutocomplete/UserOrGroupOption.tsx
deleted file mode 100644
index dd9506fc7e837..0000000000000
--- a/site/src/components/UserOrGroupAutocomplete/UserOrGroupOption.tsx
+++ /dev/null
@@ -1,43 +0,0 @@
-import type { Group, ReducedUser, User } from "api/typesGenerated";
-import { AvatarData } from "components/Avatar/AvatarData";
-import type { HTMLAttributes } from "react";
-import { getGroupSubtitle } from "utils/groups";
-
-type UserOrGroupAutocompleteValue = User | ReducedUser | Group | null;
-
-type UserOption = User | ReducedUser;
-type OptionType = UserOption | Group;
-
-/**
- * Type guard to check if the value is a Group.
- * Groups have a "members" property that users don't have.
- */
-export const isGroup = (
-	value: UserOrGroupAutocompleteValue,
-): value is Group => {
-	return value !== null && typeof value === "object" && "members" in value;
-};
-
-interface UserOrGroupOptionProps {
-	option: OptionType;
-	htmlProps: HTMLAttributes<HTMLLIElement>;
-}
-
-export const UserOrGroupOption = ({
-	option,
-	htmlProps,
-}: UserOrGroupOptionProps) => {
-	const isOptionGroup = isGroup(option);
-
-	return (
-		<li {...htmlProps}>
-			<AvatarData
-				title={
-					isOptionGroup ? option.display_name || option.name : option.username
-				}
-				subtitle={isOptionGroup ? getGroupSubtitle(option) : option.email}
-				src={option.avatar_url}
-			/>
-		</li>
-	);
-};
diff --git a/site/src/utils/groups.ts b/site/src/modules/groups.ts
similarity index 65%
rename from site/src/utils/groups.ts
rename to site/src/modules/groups.ts
index 4c456b81bf788..fc642d7769f4f 100644
--- a/site/src/utils/groups.ts
+++ b/site/src/modules/groups.ts
@@ -1,4 +1,16 @@
-import type { Group } from "api/typesGenerated";
+import type { Group, ReducedUser, User } from "api/typesGenerated";
+
+type UserOrGroupAutocompleteValue = User | ReducedUser | Group | null;
+
+/**
+ * Type guard to check if the value is a Group.
+ * Groups have a "members" property that users don't have.
+ */
+export const isGroup = (
+	value: UserOrGroupAutocompleteValue,
+): value is Group => {
+	return value !== null && typeof value === "object" && "members" in value;
+};
 
 /**
  * Returns true if the provided group is the 'Everyone' group.
diff --git a/site/src/pages/GroupsPage/GroupPage.tsx b/site/src/pages/GroupsPage/GroupPage.tsx
index 4213a0ac20400..b5a9f1940a705 100644
--- a/site/src/pages/GroupsPage/GroupPage.tsx
+++ b/site/src/pages/GroupsPage/GroupPage.tsx
@@ -53,10 +53,10 @@ import {
 	TrashIcon,
 	UserPlusIcon,
 } from "lucide-react";
+import { isEveryoneGroup } from "modules/groups";
 import { type FC, useState } from "react";
 import { useMutation, useQuery, useQueryClient } from "react-query";
 import { Link as RouterLink, useNavigate, useParams } from "react-router";
-import { isEveryoneGroup } from "utils/groups";
 import { pageTitle } from "utils/page";
 
 const GroupPage: FC = () => {
diff --git a/site/src/pages/GroupsPage/GroupSettingsPageView.tsx b/site/src/pages/GroupsPage/GroupSettingsPageView.tsx
index c99495d1c92ab..a07d1b4a10ccf 100644
--- a/site/src/pages/GroupsPage/GroupSettingsPageView.tsx
+++ b/site/src/pages/GroupsPage/GroupSettingsPageView.tsx
@@ -12,13 +12,13 @@ import { Loader } from "components/Loader/Loader";
 import { ResourcePageHeader } from "components/PageHeader/PageHeader";
 import { Spinner } from "components/Spinner/Spinner";
 import { useFormik } from "formik";
+import { isEveryoneGroup } from "modules/groups";
 import type { FC } from "react";
 import {
 	getFormHelpers,
 	nameValidator,
 	onChangeTrimmed,
 } from "utils/formUtils";
-import { isEveryoneGroup } from "utils/groups";
 import * as Yup from "yup";
 
 type FormData = {
diff --git a/site/src/pages/OrganizationSettingsPage/IdpSyncPage/IdpGroupSyncForm.tsx b/site/src/pages/OrganizationSettingsPage/IdpSyncPage/IdpGroupSyncForm.tsx
index 6f4cd9dc6630a..091ab4851dc4d 100644
--- a/site/src/pages/OrganizationSettingsPage/IdpSyncPage/IdpGroupSyncForm.tsx
+++ b/site/src/pages/OrganizationSettingsPage/IdpSyncPage/IdpGroupSyncForm.tsx
@@ -29,9 +29,9 @@ import {
 } from "components/Tooltip/Tooltip";
 import { useFormik } from "formik";
 import { Plus, Trash, TriangleAlert } from "lucide-react";
+import { isEveryoneGroup } from "modules/groups";
 import { type FC, type KeyboardEventHandler, useId, useState } from "react";
 import { docs } from "utils/docs";
-import { isEveryoneGroup } from "utils/groups";
 import { isUUID } from "utils/uuid";
 import * as Yup from "yup";
 import { ExportPolicyButton } from "./ExportPolicyButton";
diff --git a/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/TemplatePermissionsPageView.tsx b/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/TemplatePermissionsPageView.tsx
index 07047bbc3da97..6ad89ae0dbcd8 100644
--- a/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/TemplatePermissionsPageView.tsx
+++ b/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/TemplatePermissionsPageView.tsx
@@ -33,8 +33,8 @@ import {
 } from "components/Table/Table";
 import { TableLoader } from "components/TableLoader/TableLoader";
 import { EllipsisVertical, UserPlusIcon } from "lucide-react";
+import { getGroupSubtitle } from "modules/groups";
 import { type FC, useState } from "react";
-import { getGroupSubtitle } from "utils/groups";
 import {
 	UserOrGroupAutocomplete,
 	type UserOrGroupAutocompleteValue,
diff --git a/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/UserOrGroupAutocomplete.tsx b/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/UserOrGroupAutocomplete.tsx
index 23da3c2784981..8e7747b41c49b 100644
--- a/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/UserOrGroupAutocomplete.tsx
+++ b/site/src/pages/TemplateSettingsPage/TemplatePermissionsPage/UserOrGroupAutocomplete.tsx
@@ -1,14 +1,10 @@
-import Autocomplete from "@mui/material/Autocomplete";
-import CircularProgress from "@mui/material/CircularProgress";
-import TextField from "@mui/material/TextField";
 import { templaceACLAvailable } from "api/queries/templates";
 import type { Group, ReducedUser } from "api/typesGenerated";
-import {
-	isGroup,
-	UserOrGroupOption,
-} from "components/UserOrGroupAutocomplete/UserOrGroupOption";
-import { useDebouncedFunction } from "hooks/debounce";
-import { type ChangeEvent, type FC, useState } from "react";
+import { Autocomplete } from "components/Autocomplete/Autocomplete";
+import { AvatarData } from "components/Avatar/AvatarData";
+import { Check } from "lucide-react";
+import { getGroupSubtitle, isGroup } from "modules/groups";
+import { type FC, useState } from "react";
 import { keepPreviousData, useQuery } from "react-query";
 import { prepareQuery } from "utils/filters";
 
@@ -28,18 +24,25 @@ export const UserOrGroupAutocomplete: FC<UserOrGroupAutocompleteProps> = ({
 	templateID,
 	exclude,
 }) => {
-	const [autoComplete, setAutoComplete] = useState({
-		value: "",
-		open: false,
-	});
+	const [inputValue, setInputValue] = useState("");
+	const [open, setOpen] = useState(false);
+
+	const handleOpenChange = (newOpen: boolean) => {
+		setOpen(newOpen);
+		if (!newOpen) {
+			setInputValue("");
+		}
+	};
+
 	const aclAvailableQuery = useQuery({
 		...templaceACLAvailable(templateID, {
-			q: prepareQuery(encodeURI(autoComplete.value)),
+			q: prepareQuery(encodeURI(inputValue)),
 			limit: 25,
 		}),
-		enabled: autoComplete.open,
+		enabled: open,
 		placeholderData: keepPreviousData,
 	});
+
 	const options: AutocompleteOption[] = aclAvailableQuery.data
 		? [
 				...aclAvailableQuery.data.groups,
@@ -52,69 +55,41 @@ export const UserOrGroupAutocomplete: FC<UserOrGroupAutocompleteProps> = ({
 			})
 		: [];
 
-	const { debounced: handleFilterChange } = useDebouncedFunction(
-		(event: ChangeEvent<HTMLInputElement>) => {
-			setAutoComplete((state) => ({
-				...state,
-				value: event.target.value,
-			}));
-		},
-		500,
-	);
-
 	return (
 		<Autocomplete
-			noOptionsText="No users or groups found"
 			value={value}
-			id="user-or-group-autocomplete"
-			open={autoComplete.open}
-			onOpen={() => {
-				setAutoComplete((state) => ({
-					...state,
-					open: true,
-				}));
-			}}
-			onClose={() => {
-				setAutoComplete({
-					value: isGroup(value) ? value.display_name : (value?.email ?? ""),
-					open: false,
-				});
-			}}
-			onChange={(_, newValue) => {
-				onChange(newValue);
-			}}
-			isOptionEqualToValue={(option, optionValue) =>
-				option.id === optionValue.id
-			}
+			onChange={onChange}
+			options={options}
+			getOptionValue={(option) => option.id}
 			getOptionLabel={(option) =>
 				isGroup(option) ? option.display_name || option.name : option.email
 			}
-			renderOption={({ key, ...props }, option) => (
-				<UserOrGroupOption key={key} htmlProps={props} option={option} />
+			isOptionEqualToValue={(option, optionValue) =>
+				option.id === optionValue.id
+			}
+			renderOption={(option, isSelected) => (
+				<div className="flex items-center justify-between w-full">
+					<AvatarData
+						title={
+							isGroup(option)
+								? option.display_name || option.name
+								: option.username
+						}
+						subtitle={isGroup(option) ? getGroupSubtitle(option) : option.email}
+						src={option.avatar_url}
+					/>
+					{isSelected && <Check className="size-4 shrink-0" />}
+				</div>
 			)}
-			options={options}
+			open={open}
+			onOpenChange={handleOpenChange}
+			inputValue={inputValue}
+			onInputChange={setInputValue}
 			loading={aclAvailableQuery.isFetching}
-			className="w-[300px] [&_.MuiFormControl-root]:w-full [&_.MuiInputBase-root]:w-full"
-			renderInput={(params) => (
-				<TextField
-					{...params}
-					margin="none"
-					size="small"
-					placeholder="Search for user or group"
-					InputProps={{
-						...params.InputProps,
-						onChange: handleFilterChange,
-						endAdornment: (
-							<>
-								{aclAvailableQuery.isFetching ? (
-									<CircularProgress size={16} />
-								) : null}
-								{params.InputProps.endAdornment}
-							</>
-						),
-					}}
-				/>
-			)}
+			placeholder="Search for user or group"
+			noOptionsText="No users or groups found"
+			className="w-[300px]"
+			id="user-or-group-autocomplete"
 		/>
 	);
 };
diff --git a/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/UserOrGroupAutocomplete.tsx b/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/UserOrGroupAutocomplete.tsx
index 8e61f92b2cd41..86b5546d6c5d1 100644
--- a/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/UserOrGroupAutocomplete.tsx
+++ b/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/UserOrGroupAutocomplete.tsx
@@ -1,15 +1,11 @@
-import Autocomplete from "@mui/material/Autocomplete";
-import CircularProgress from "@mui/material/CircularProgress";
-import TextField from "@mui/material/TextField";
 import { groupsByOrganization } from "api/queries/groups";
 import { users } from "api/queries/users";
 import type { Group, User } from "api/typesGenerated";
-import {
-	isGroup,
-	UserOrGroupOption,
-} from "components/UserOrGroupAutocomplete/UserOrGroupOption";
-import { useDebouncedFunction } from "hooks/debounce";
-import { type ChangeEvent, type FC, useState } from "react";
+import { Autocomplete } from "components/Autocomplete/Autocomplete";
+import { AvatarData } from "components/Avatar/AvatarData";
+import { Check } from "lucide-react";
+import { getGroupSubtitle, isGroup } from "modules/groups";
+import { type FC, useState } from "react";
 import { keepPreviousData, useQuery } from "react-query";
 import { prepareQuery } from "utils/filters";
 
@@ -31,27 +27,32 @@ export const UserOrGroupAutocomplete: FC<UserOrGroupAutocompleteProps> = ({
 	organizationId,
 	exclude,
 }) => {
-	const [autoComplete, setAutoComplete] = useState({
-		value: "",
-		open: false,
-	});
+	const [inputValue, setInputValue] = useState("");
+	const [open, setOpen] = useState(false);
+
+	const handleOpenChange = (newOpen: boolean) => {
+		setOpen(newOpen);
+		if (!newOpen) {
+			setInputValue("");
+		}
+	};
 
 	const usersQuery = useQuery({
 		...users({
-			q: prepareQuery(encodeURI(autoComplete.value)),
+			q: prepareQuery(encodeURI(inputValue)),
 			limit: 25,
 		}),
-		enabled: autoComplete.open,
+		enabled: open,
 		placeholderData: keepPreviousData,
 	});
 
 	const groupsQuery = useQuery({
 		...groupsByOrganization(organizationId),
-		enabled: autoComplete.open,
+		enabled: open,
 		placeholderData: keepPreviousData,
 	});
 
-	const filterValue = autoComplete.value.trim().toLowerCase();
+	const filterValue = inputValue.trim().toLowerCase();
 	const groupOptions = groupsQuery.data
 		? groupsQuery.data.filter((group) => {
 				if (!filterValue) {
@@ -71,71 +72,41 @@ export const UserOrGroupAutocomplete: FC<UserOrGroupAutocompleteProps> = ({
 		...(usersQuery.data?.users ?? []),
 	].filter((result) => !excludeIds.includes(result.id));
 
-	const { debounced: handleFilterChange } = useDebouncedFunction(
-		(event: ChangeEvent<HTMLInputElement>) => {
-			setAutoComplete((state) => ({
-				...state,
-				value: event.target.value,
-			}));
-		},
-		500,
-	);
-
 	return (
 		<Autocomplete
-			noOptionsText="No users or groups found"
 			value={value}
-			id="workspace-user-or-group-autocomplete"
-			open={autoComplete.open}
-			onOpen={() => {
-				setAutoComplete((state) => ({
-					...state,
-					open: true,
-				}));
-			}}
-			onClose={() => {
-				setAutoComplete({
-					value: isGroup(value)
-						? value.display_name || value.name
-						: (value?.email ?? value?.username ?? ""),
-					open: false,
-				});
-			}}
-			onChange={(_, newValue) => {
-				onChange(newValue ?? null);
-			}}
-			isOptionEqualToValue={(option, optionValue) =>
-				option.id === optionValue.id
-			}
+			onChange={onChange}
+			options={options}
+			getOptionValue={(option) => option.id}
 			getOptionLabel={(option) =>
 				isGroup(option) ? option.display_name || option.name : option.email
 			}
-			renderOption={({ key, ...props }, option) => (
-				<UserOrGroupOption key={key} htmlProps={props} option={option} />
+			isOptionEqualToValue={(option, optionValue) =>
+				option.id === optionValue.id
+			}
+			renderOption={(option, isSelected) => (
+				<div className="flex items-center justify-between w-full">
+					<AvatarData
+						title={
+							isGroup(option)
+								? option.display_name || option.name
+								: option.username
+						}
+						subtitle={isGroup(option) ? getGroupSubtitle(option) : option.email}
+						src={option.avatar_url}
+					/>
+					{isSelected && <Check className="size-4 shrink-0" />}
+				</div>
 			)}
-			options={options}
+			open={open}
+			onOpenChange={handleOpenChange}
+			inputValue={inputValue}
+			onInputChange={setInputValue}
 			loading={usersQuery.isFetching || groupsQuery.isFetching}
-			className="w-[300px] [&_.MuiFormControl-root]:w-full [&_.MuiInputBase-root]:w-full"
-			renderInput={(params) => (
-				<TextField
-					{...params}
-					margin="none"
-					size="small"
-					placeholder="Search for user or group"
-					InputProps={{
-						...params.InputProps,
-						onChange: handleFilterChange,
-						endAdornment: (
-							<>
-								{(usersQuery.isFetching || groupsQuery.isFetching) && (
-									<CircularProgress size={16} />
-								)}
-								{params.InputProps.endAdornment}
-							</>
-						),
-					}}
-				/>
-			)}
+			placeholder="Search for user or group"
+			noOptionsText="No users or groups found"
+			className="w-80"
+			id="workspace-user-or-group-autocomplete"
 		/>
 	);
 };
diff --git a/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/WorkspaceSharingPageView.tsx b/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/WorkspaceSharingPageView.tsx
index 403480d19e1b8..c4fe8a2cc5eff 100644
--- a/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/WorkspaceSharingPageView.tsx
+++ b/site/src/pages/WorkspaceSettingsPage/WorkspaceSharingPage/WorkspaceSharingPageView.tsx
@@ -35,8 +35,8 @@ import {
 } from "components/Table/Table";
 import { TableLoader } from "components/TableLoader/TableLoader";
 import { EllipsisVertical, UserPlusIcon } from "lucide-react";
+import { getGroupSubtitle } from "modules/groups";
 import { type FC, useState } from "react";
-import { getGroupSubtitle } from "utils/groups";
 import {
 	UserOrGroupAutocomplete,
 	type UserOrGroupAutocompleteValue,