diff --git a/src/components/views/rooms/RoomListHeader.tsx b/src/components/views/rooms/RoomListHeader.tsx
index 6b97e8a660..6a892df238 100644
--- a/src/components/views/rooms/RoomListHeader.tsx
+++ b/src/components/views/rooms/RoomListHeader.tsx
@@ -140,6 +140,15 @@ const RoomListHeader = ({ onVisibilityChange }: IProps) => {
         }
     });
 
+    const canShowMainMenu = activeSpace || spaceKey === MetaSpace.Home;
+
+    useEffect(() => {
+        if (mainMenuDisplayed && !canShowMainMenu) {
+            // Space changed under us and we no longer has a main menu to draw
+            closeMainMenu();
+        }
+    }, [closeMainMenu, canShowMainMenu, mainMenuDisplayed]);
+
     // we pass null for the queryLength to inhibit the metrics hook for when there is no filterCondition
     useWebSearchMetrics(count, filterCondition ? filterCondition.search.length : null, false);
 
@@ -168,7 +177,7 @@ const RoomListHeader = ({ onVisibilityChange }: IProps) => {
     const canShowPlusMenu = canCreateRooms || canExploreRooms || activeSpace;
 
     let contextMenu: JSX.Element;
-    if (mainMenuDisplayed) {
+    if (mainMenuDisplayed && mainMenuHandle.current) {
         let ContextMenuComponent;
         if (activeSpace) {
             ContextMenuComponent = SpaceContextMenu;
@@ -364,7 +373,7 @@ const RoomListHeader = ({ onVisibilityChange }: IProps) => {
         .join("\n");
 
     let contextMenuButton: JSX.Element = <div className="mx_RoomListHeader_contextLessTitle">{ title }</div>;
-    if (activeSpace || spaceKey === MetaSpace.Home) {
+    if (canShowMainMenu) {
         contextMenuButton = <ContextMenuTooltipButton
             inputRef={mainMenuHandle}
             onClick={openMainMenu}
diff --git a/test/components/views/rooms/RoomListHeader-test.tsx b/test/components/views/rooms/RoomListHeader-test.tsx
new file mode 100644
index 0000000000..1baabebbb8
--- /dev/null
+++ b/test/components/views/rooms/RoomListHeader-test.tsx
@@ -0,0 +1,136 @@
+/*
+Copyright 2022 The Matrix.org Foundation C.I.C.
+
+Licensed under the Apache License, Version 2.0 (the "License");
+you may not use this file except in compliance with the License.
+You may obtain a copy of the License at
+
+    http://www.apache.org/licenses/LICENSE-2.0
+
+Unless required by applicable law or agreed to in writing, software
+distributed under the License is distributed on an "AS IS" BASIS,
+WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+See the License for the specific language governing permissions and
+limitations under the License.
+*/
+
+import React from 'react';
+import { mount } from 'enzyme';
+import { MatrixClient } from 'matrix-js-sdk/src/client';
+import { act } from "react-dom/test-utils";
+
+import SpaceStore from "../../../../src/stores/spaces/SpaceStore";
+import { MetaSpace } from "../../../../src/stores/spaces";
+import RoomListHeader from "../../../../src/components/views/rooms/RoomListHeader";
+import * as testUtils from "../../../test-utils";
+import { createTestClient, mkSpace } from "../../../test-utils";
+import DMRoomMap from "../../../../src/utils/DMRoomMap";
+import MatrixClientContext from "../../../../src/contexts/MatrixClientContext";
+import SettingsStore from "../../../../src/settings/SettingsStore";
+import { SettingLevel } from "../../../../src/settings/SettingLevel";
+
+describe("RoomListHeader", () => {
+    let client: MatrixClient;
+
+    beforeEach(() => {
+        client = createTestClient();
+    });
+
+    it("renders a main menu for the home space", () => {
+        act(() => {
+            SpaceStore.instance.setActiveSpace(MetaSpace.Home);
+        });
+
+        const wrapper = mount(<MatrixClientContext.Provider value={client}>
+            <RoomListHeader />
+        </MatrixClientContext.Provider>);
+
+        expect(wrapper.text()).toBe("Home");
+        act(() => {
+            wrapper.find('[aria-label="Home options"]').hostNodes().simulate("click");
+        });
+        wrapper.update();
+
+        const menu = wrapper.find(".mx_IconizedContextMenu");
+        const items = menu.find(".mx_IconizedContextMenu_item").hostNodes();
+        expect(items).toHaveLength(1);
+        expect(items.at(0).text()).toBe("Show all rooms");
+    });
+
+    it("renders a main menu for spaces", async () => {
+        const testSpace = mkSpace(client, "!space:server");
+        testSpace.name = "Test Space";
+        client.getRoom = () => testSpace;
+
+        const getUserIdForRoomId = jest.fn();
+        const getDMRoomsForUserId = jest.fn();
+        // @ts-ignore
+        DMRoomMap.sharedInstance = { getUserIdForRoomId, getDMRoomsForUserId };
+
+        await testUtils.setupAsyncStoreWithClient(SpaceStore.instance, client);
+        act(() => {
+            SpaceStore.instance.setActiveSpace(testSpace.roomId);
+        });
+
+        const wrapper = mount(<MatrixClientContext.Provider value={client}>
+            <RoomListHeader />
+        </MatrixClientContext.Provider>);
+
+        expect(wrapper.text()).toBe("Test Space");
+        act(() => {
+            wrapper.find('[aria-label="Test Space menu"]').hostNodes().simulate("click");
+        });
+        wrapper.update();
+
+        const menu = wrapper.find(".mx_IconizedContextMenu");
+        const items = menu.find(".mx_IconizedContextMenu_item").hostNodes();
+        expect(items).toHaveLength(6);
+        expect(items.at(0).text()).toBe("Space home");
+        expect(items.at(1).text()).toBe("Manage & explore rooms");
+        expect(items.at(2).text()).toBe("Preferences");
+        expect(items.at(3).text()).toBe("Settings");
+        expect(items.at(4).text()).toBe("Room");
+        expect(items.at(4).text()).toBe("Room");
+    });
+
+    it("closes menu if space changes from under it", async () => {
+        await SettingsStore.setValue("Spaces.enabledMetaSpaces", null, SettingLevel.DEVICE, {
+            [MetaSpace.Home]: true,
+            [MetaSpace.Favourites]: true,
+        });
+
+        const testSpace = mkSpace(client, "!space:server");
+        testSpace.name = "Test Space";
+        client.getRoom = () => testSpace;
+
+        const getUserIdForRoomId = jest.fn();
+        const getDMRoomsForUserId = jest.fn();
+        // @ts-ignore
+        DMRoomMap.sharedInstance = { getUserIdForRoomId, getDMRoomsForUserId };
+
+        await testUtils.setupAsyncStoreWithClient(SpaceStore.instance, client);
+        act(() => {
+            SpaceStore.instance.setActiveSpace(testSpace.roomId);
+        });
+
+        const wrapper = mount(<MatrixClientContext.Provider value={client}>
+            <RoomListHeader />
+        </MatrixClientContext.Provider>);
+
+        expect(wrapper.text()).toBe("Test Space");
+        act(() => {
+            wrapper.find('[aria-label="Test Space menu"]').hostNodes().simulate("click");
+        });
+        wrapper.update();
+
+        act(() => {
+            SpaceStore.instance.setActiveSpace(MetaSpace.Favourites);
+        });
+        wrapper.update();
+
+        expect(wrapper.text()).toBe("Favourites");
+
+        const menu = wrapper.find(".mx_IconizedContextMenu");
+        expect(menu).toHaveLength(0);
+    });
+});
diff --git a/test/test-utils/test-utils.ts b/test/test-utils/test-utils.ts
index 14bd85bc5c..fc85a825f3 100644
--- a/test/test-utils/test-utils.ts
+++ b/test/test-utils/test-utils.ts
@@ -379,6 +379,7 @@ export function mkStubRoom(roomId: string = null, name: string, client: MatrixCl
         getJoinRule: jest.fn().mockReturnValue("invite"),
         loadMembersIfNeeded: jest.fn(),
         client,
+        canInvite: jest.fn(),
     } as unknown as Room;
 }