diff --git a/site/src/pages/AgentsPage/components/AgentCreateForm.stories.tsx b/site/src/pages/AgentsPage/components/AgentCreateForm.stories.tsx
index 201bea72e2..bc72dca99b 100644
--- a/site/src/pages/AgentsPage/components/AgentCreateForm.stories.tsx
+++ b/site/src/pages/AgentsPage/components/AgentCreateForm.stories.tsx
@@ -338,9 +338,7 @@ export const WithOrganizationPicker: Story = {
 		const canvas = within(canvasElement);
 		// Verify the org picker rendered (component didn't crash).
 		await waitFor(() => {
-			expect(
-				canvas.getByTestId("organization-autocomplete"),
-			).toBeInTheDocument();
+			expect(canvas.getByTestId("compact-org-selector")).toBeInTheDocument();
 		});
 		// Type into the chat input to trigger re-renders. If the
 		// permittedOrgs fallback is referentially unstable, this
@@ -349,7 +347,7 @@ export const WithOrganizationPicker: Story = {
 		await userEvent.click(input);
 		await userEvent.keyboard("hello world");
 		// The org picker should still be present after typing.
-		expect(canvas.getByTestId("organization-autocomplete")).toBeInTheDocument();
+		expect(canvas.getByTestId("compact-org-selector")).toBeInTheDocument();
 	},
 };
 
diff --git a/site/src/pages/AgentsPage/components/AgentCreateForm.tsx b/site/src/pages/AgentsPage/components/AgentCreateForm.tsx
index 55bac24262..a09ffa8d88 100644
--- a/site/src/pages/AgentsPage/components/AgentCreateForm.tsx
+++ b/site/src/pages/AgentsPage/components/AgentCreateForm.tsx
@@ -9,8 +9,6 @@ import { Alert, AlertDescription } from "#/components/Alert/Alert";
 import { ErrorAlert } from "#/components/Alert/ErrorAlert";
 import { Button } from "#/components/Button/Button";
 import { ConfirmDialog } from "#/components/Dialogs/ConfirmDialog/ConfirmDialog";
-import { Label } from "#/components/Label/Label";
-import { OrganizationAutocomplete } from "#/components/OrganizationAutocomplete/OrganizationAutocomplete";
 import { useDashboard } from "#/modules/dashboard/useDashboard";
 import { docs } from "#/utils/docs";
 import { useFileAttachments } from "../hooks/useFileAttachments";
@@ -27,6 +25,7 @@ import {
 import { AgentChatInput } from "./AgentChatInput";
 import { ChatAccessDeniedAlert } from "./ChatAccessDeniedAlert";
 import type { ModelSelectorOption } from "./ChatElements";
+import { CompactOrgSelector } from "./ChatElements";
 import {
 	getDefaultMCPSelection,
 	getSavedMCPSelection,
@@ -433,30 +432,23 @@ export const AgentCreateForm: FC<AgentCreateFormProps> = ({
 					{permittedOrgsQuery.error != null && (
 						<ErrorAlert error={permittedOrgsQuery.error} />
 					)}
-					{showOrganizations &&
-						!permittedOrgsQuery.isLoading &&
-						permittedOrgs.length > 1 && (
-							<div className="flex flex-col gap-2">
-								<Label htmlFor="organization">Organization</Label>
-								<OrganizationAutocomplete
-									id="organization"
-									required
-									value={selectedOrg}
-									options={permittedOrgs}
-									onChange={(newOrg) => {
-										const orgChanged = newOrg?.id !== selectedOrg?.id;
-										if (orgChanged && attachments.length > 0) {
-											setPendingOrgChange(newOrg);
-											return;
-										}
-										if (orgChanged) {
-											handleWorkspaceChange(null);
-										}
-										setSelectedOrg(newOrg);
-									}}
-								/>
-							</div>
-						)}
+					{showOrganizations && permittedOrgs.length > 1 && (
+						<CompactOrgSelector
+							value={selectedOrg}
+							options={permittedOrgs}
+							onChange={(newOrg) => {
+								const orgChanged = newOrg.id !== selectedOrg?.id;
+								if (orgChanged && attachments.length > 0) {
+									setPendingOrgChange(newOrg);
+									return;
+								}
+								if (orgChanged) {
+									handleWorkspaceChange(null);
+								}
+								setSelectedOrg(newOrg);
+							}}
+						/>
+					)}
 					<AgentChatInput
 						onSend={handleSendWithAttachments}
 						placeholder="Ask Coder to build, fix bugs, or explore your project..."
diff --git a/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.stories.tsx b/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.stories.tsx
new file mode 100644
index 0000000000..8c75d4a72d
--- /dev/null
+++ b/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.stories.tsx
@@ -0,0 +1,79 @@
+import type { Meta, StoryObj } from "@storybook/react-vite";
+import { fn } from "storybook/test";
+import type { Organization } from "#/api/typesGenerated";
+import { CompactOrgSelector } from "./CompactOrgSelector";
+
+const mockOrgs: Organization[] = [
+	{
+		id: "org-coder",
+		name: "coder",
+		display_name: "Coder",
+		icon: "/icon/coder.svg",
+		description: "Main engineering organization",
+		created_at: "2024-01-01T00:00:00Z",
+		updated_at: "2024-06-01T00:00:00Z",
+		is_default: true,
+	},
+	{
+		id: "org-acme",
+		name: "acme-corp",
+		display_name: "Acme Corp",
+		icon: "",
+		description: "Acme Corporation",
+		created_at: "2024-02-01T00:00:00Z",
+		updated_at: "2024-06-01T00:00:00Z",
+		is_default: false,
+	},
+	{
+		id: "org-globex",
+		name: "globex",
+		display_name: "Globex Inc",
+		icon: "",
+		description: "Globex Incorporated",
+		created_at: "2024-03-01T00:00:00Z",
+		updated_at: "2024-06-01T00:00:00Z",
+		is_default: false,
+	},
+];
+
+const meta: Meta<typeof CompactOrgSelector> = {
+	title: "pages/AgentsPage/ChatElements/CompactOrgSelector",
+	component: CompactOrgSelector,
+	decorators: [
+		(Story) => (
+			<div className="w-72 rounded-lg border border-solid border-border-default bg-surface-primary p-4">
+				<Story />
+			</div>
+		),
+	],
+	args: {
+		options: mockOrgs,
+		value: mockOrgs[0],
+		onChange: fn(),
+	},
+};
+
+export default meta;
+type Story = StoryObj<typeof CompactOrgSelector>;
+
+export const Default: Story = {};
+
+export const Disabled: Story = {
+	args: {
+		disabled: true,
+		value: mockOrgs[0],
+	},
+};
+
+export const NoSelection: Story = {
+	args: {
+		value: null,
+	},
+};
+
+export const SingleOption: Story = {
+	args: {
+		options: [mockOrgs[0]],
+		value: mockOrgs[0],
+	},
+};
diff --git a/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.tsx b/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.tsx
new file mode 100644
index 0000000000..572b62c304
--- /dev/null
+++ b/site/src/pages/AgentsPage/components/ChatElements/CompactOrgSelector.tsx
@@ -0,0 +1,126 @@
+import { Check } from "lucide-react";
+import { type FC, useState } from "react";
+import type { Organization } from "#/api/typesGenerated";
+import { ChevronDownIcon } from "#/components/AnimatedIcons/ChevronDown";
+import { Avatar } from "#/components/Avatar/Avatar";
+import {
+	Command,
+	CommandEmpty,
+	CommandGroup,
+	CommandInput,
+	CommandItem,
+	CommandList,
+} from "#/components/Command/Command";
+import {
+	Popover,
+	PopoverContent,
+	PopoverTrigger,
+} from "#/components/Popover/Popover";
+import { cn } from "#/utils/cn";
+
+interface CompactOrgSelectorProps {
+	value: Organization | null;
+	onChange?: (organization: Organization) => void;
+	options: readonly Organization[];
+	disabled?: boolean;
+	className?: string;
+	dropdownSide?: "top" | "bottom" | "left" | "right";
+	dropdownAlign?: "start" | "center" | "end";
+}
+
+export const CompactOrgSelector: FC<CompactOrgSelectorProps> = ({
+	value,
+	onChange,
+	options,
+	disabled = false,
+	className,
+	dropdownSide = "bottom",
+	dropdownAlign = "start",
+}) => {
+	const [open, setOpen] = useState(false);
+	const isDisabled = disabled || options.length === 0;
+
+	return (
+		<Popover open={open} onOpenChange={isDisabled ? undefined : setOpen}>
+			<PopoverTrigger asChild>
+				<button
+					type="button"
+					disabled={isDisabled}
+					data-testid="compact-org-selector"
+					aria-label={
+						value
+							? `Organization: ${value.display_name || value.name}`
+							: "Select organization"
+					}
+					className={cn(
+						"group flex h-6 w-auto cursor-pointer items-center gap-1.5 border-none bg-transparent px-1 text-xs text-content-secondary shadow-none whitespace-nowrap transition-colors",
+						"hover:text-content-primary focus:ring-0",
+						"disabled:cursor-not-allowed disabled:opacity-50",
+						className,
+					)}
+				>
+					{value ? (
+						<>
+							<Avatar
+								size="sm"
+								src={value.icon}
+								fallback={value.display_name || value.name}
+								className="!size-3.5 border-0"
+							/>
+							<span className="truncate">
+								{value.display_name || value.name}
+							</span>
+						</>
+					) : (
+						<span>Select org…</span>
+					)}
+					<ChevronDownIcon
+						open={open}
+						className="size-icon-sm shrink-0 text-content-secondary transition-colors hover:text-content-primary group-hover:text-content-primary"
+					/>
+				</button>
+			</PopoverTrigger>
+			<PopoverContent
+				side={dropdownSide}
+				align={dropdownAlign}
+				className="w-64 p-0"
+			>
+				<Command loop>
+					<CommandInput placeholder="Find organization…" className="text-xs" />
+					<CommandList>
+						<CommandEmpty className="text-xs">
+							No organizations found
+						</CommandEmpty>
+						<CommandGroup>
+							{options.map((org) => (
+								<CommandItem
+									className="text-xs font-normal"
+									key={org.id}
+									value={`${org.display_name} ${org.name}`}
+									onSelect={() => {
+										onChange?.(org);
+										setOpen(false);
+									}}
+								>
+									{" "}
+									<Avatar
+										size="sm"
+										src={org.icon}
+										fallback={org.display_name || org.name}
+										className="!size-3.5 border-0"
+									/>
+									<span className="truncate">
+										{org.display_name || org.name}
+									</span>
+									{value?.id === org.id && (
+										<Check className="ml-auto size-icon-sm shrink-0" />
+									)}
+								</CommandItem>
+							))}
+						</CommandGroup>
+					</CommandList>
+				</Command>
+			</PopoverContent>
+		</Popover>
+	);
+};
diff --git a/site/src/pages/AgentsPage/components/ChatElements/index.ts b/site/src/pages/AgentsPage/components/ChatElements/index.ts
index f7435961e5..fb5c6c4875 100644
--- a/site/src/pages/AgentsPage/components/ChatElements/index.ts
+++ b/site/src/pages/AgentsPage/components/ChatElements/index.ts
@@ -1,3 +1,4 @@
+export { CompactOrgSelector } from "./CompactOrgSelector";
 export { ConversationItem } from "./Conversation";
 export { Message, MessageContent } from "./Message";
 export type { ModelSelectorOption } from "./ModelSelector";
diff --git a/site/src/pages/AgentsPage/components/ChatPageContent.tsx b/site/src/pages/AgentsPage/components/ChatPageContent.tsx
index 76d4ac3e17..f171826fc7 100644
--- a/site/src/pages/AgentsPage/components/ChatPageContent.tsx
+++ b/site/src/pages/AgentsPage/components/ChatPageContent.tsx
@@ -422,9 +422,11 @@ export const ChatPageInput: FC<ChatPageInputProps> = ({
 	return (
 		<div>
 			{inputElement}
-			<div className="px-3 pt-1 text-2xs text-content-secondary">
-				{modelSelectorHelp}
-			</div>
+			{modelSelectorHelp && (
+				<div className="px-3 pt-1 text-2xs text-content-secondary">
+					{modelSelectorHelp}
+				</div>
+			)}
 		</div>
 	);
 };