diff --git a/webapp/channels/src/utils/popouts/popout_windows.test.ts b/webapp/channels/src/utils/popouts/popout_windows.test.ts
index efe60e6ca78..a9948aab5e0 100644
--- a/webapp/channels/src/utils/popouts/popout_windows.test.ts
+++ b/webapp/channels/src/utils/popouts/popout_windows.test.ts
@@ -2,6 +2,7 @@
 // See LICENSE.txt for license information.
 
 import DesktopApp from 'utils/desktop_api';
+import {getBasePath} from 'utils/url';
 import {isDesktopApp} from 'utils/user_agent';
 
 import {FOCUS_REPLY_POST, popoutRhsPlugin, popoutThread} from './popout_windows';
@@ -20,6 +21,10 @@ jest.mock('utils/user_agent', () => ({
     isDesktopApp: jest.fn(),
 }));
 
+jest.mock('utils/url', () => ({
+    getBasePath: jest.fn(),
+}));
+
 jest.mock('./browser_popouts', () => {
     const mockFn = jest.fn();
     (globalThis as typeof globalThis & {mockSetupBrowserPopout: typeof mockFn}).mockSetupBrowserPopout = mockFn;
@@ -33,6 +38,7 @@ jest.mock('./browser_popouts', () => {
 
 const mockDesktopApp = DesktopApp as jest.Mocked<typeof DesktopApp>;
 const mockIsDesktopApp = isDesktopApp as jest.MockedFunction<typeof isDesktopApp>;
+const mockGetBasePath = getBasePath as jest.MockedFunction<typeof getBasePath>;
 
 const getMockSetupBrowserPopout = () => {
     return (globalThis as typeof globalThis & {mockSetupBrowserPopout: jest.MockedFunction<() => unknown>}).mockSetupBrowserPopout;
@@ -42,6 +48,9 @@ describe('popout_windows', () => {
     beforeEach(() => {
         jest.clearAllMocks();
         getMockSetupBrowserPopout().mockClear();
+
+        // Default: no subpath
+        mockGetBasePath.mockReturnValue('');
     });
 
     describe('popoutThread', () => {
@@ -121,6 +130,23 @@ describe('popout_windows', () => {
             expect(mockOnFocusPost).toHaveBeenCalledTimes(1);
             expect(mockOnFocusPost).toHaveBeenCalledWith('post-123', '/team/pl/post-123');
         });
+
+        it('should include subpath in popout URL when basename is set', async () => {
+            mockIsDesktopApp.mockReturnValue(false);
+            mockGetBasePath.mockReturnValue('/company/mattermost');
+            const mockListeners = {
+                sendToPopout: jest.fn(),
+                onMessageFromPopout: jest.fn(),
+                onClosePopout: jest.fn(),
+            };
+            getMockSetupBrowserPopout().mockReturnValue(mockListeners);
+
+            await popoutThread('Thread - {channelName} - {teamName} - {serverName}', 'thread-123', 'test-team', mockOnFocusPost);
+
+            expect(getMockSetupBrowserPopout()).toHaveBeenCalledWith(
+                '/company/mattermost/_popout/thread/test-team/thread-123',
+            );
+        });
     });
 
     describe('popoutRhsPlugin', () => {
@@ -173,6 +199,23 @@ describe('popout_windows', () => {
 
             expect(result).toEqual(mockListeners);
         });
+
+        it('should include subpath in popout URL when basename is set', async () => {
+            mockIsDesktopApp.mockReturnValue(false);
+            mockGetBasePath.mockReturnValue('/company/mattermost');
+            const mockListeners = {
+                sendToPopout: jest.fn(),
+                onMessageFromPopout: jest.fn(),
+                onClosePopout: jest.fn(),
+            };
+            getMockSetupBrowserPopout().mockReturnValue(mockListeners);
+
+            await popoutRhsPlugin('{pluginDisplayName} - {serverName}', 'test-plugin-id', 'test-team', 'test-channel');
+
+            expect(getMockSetupBrowserPopout()).toHaveBeenCalledWith(
+                '/company/mattermost/_popout/rhs/test-team/test-channel/plugin/test-plugin-id',
+            );
+        });
     });
 });
 
diff --git a/webapp/channels/src/utils/popouts/popout_windows.ts b/webapp/channels/src/utils/popouts/popout_windows.ts
index 55290eb51e4..4f7988aa47f 100644
--- a/webapp/channels/src/utils/popouts/popout_windows.ts
+++ b/webapp/channels/src/utils/popouts/popout_windows.ts
@@ -6,6 +6,7 @@ import type {PopoutViewProps} from '@mattermost/desktop-api';
 import {Client4} from 'mattermost-redux/client';
 
 import DesktopApp from 'utils/desktop_api';
+import {getBasePath} from 'utils/url';
 import {isDesktopApp} from 'utils/user_agent';
 
 import BrowserPopouts from './browser_popouts';
@@ -27,7 +28,7 @@ export async function popoutThread(
     onFocusPost: (postId: string, returnTo: string) => void,
 ) {
     const popoutListeners = await popout(
-        `/_popout/thread/${teamName}/${threadId}`,
+        `${getBasePath()}/_popout/thread/${teamName}/${threadId}`,
         {
             isRHS: true,
             titleTemplate,
@@ -54,7 +55,7 @@ export async function popoutRhsPlugin(
     channelName: string,
 ) {
     const listeners = await popout(
-        `/_popout/rhs/${teamName}/${channelName}/plugin/${pluginId}`,
+        `${getBasePath()}/_popout/rhs/${teamName}/${channelName}/plugin/${pluginId}`,
         {
             isRHS: true,
             titleTemplate,