diff --git a/apps/meteor/client/views/room/Header/RoomHeader.spec.tsx b/apps/meteor/client/views/room/Header/RoomHeader.spec.tsx
index 3db80cf37ce76..42fb618869da1 100644
--- a/apps/meteor/client/views/room/Header/RoomHeader.spec.tsx
+++ b/apps/meteor/client/views/room/Header/RoomHeader.spec.tsx
@@ -1,11 +1,14 @@
 import { mockAppRoot } from '@rocket.chat/mock-providers';
+import { LayoutContext, RoomToolboxContext } from '@rocket.chat/ui-contexts';
+import type { RoomToolboxActionConfig, LayoutContextValue } from '@rocket.chat/ui-contexts';
 import { render, screen } from '@testing-library/react';
+import { axe } from 'jest-axe';
 
 import RoomHeader from './RoomHeader';
 import FakeRoomProvider from '../../../../tests/mocks/client/FakeRoomProvider';
 import { createFakeRoom } from '../../../../tests/mocks/data';
 
-const mockedRoom = createFakeRoom({ prid: undefined });
+const mockedRoom = createFakeRoom({ prid: undefined, name: 'general', fname: 'General' });
 const appRoot = mockAppRoot()
 	.withRoom(mockedRoom)
 	.wrap((children) => <FakeRoomProvider roomOverrides={mockedRoom}>{children}</FakeRoomProvider>)
@@ -20,10 +23,37 @@ jest.mock('./ParentRoom', () => ({
 	default: jest.fn(() => <div>ParentRoom</div>),
 }));
 
-jest.mock('./RoomToolbox', () => ({
-	__esModule: true,
-	default: jest.fn(() => <div>RoomToolbox</div>),
-}));
+const mockUseRealRoomToolbox = { value: false };
+
+jest.mock('./RoomToolbox', () => {
+	const ActualRoomToolbox = jest.requireActual('./RoomToolbox/RoomToolbox').default;
+	return {
+		__esModule: true,
+		default: jest.fn((props) => {
+			if (mockUseRealRoomToolbox.value) {
+				return <ActualRoomToolbox {...props} />;
+			}
+			return <div>RoomToolbox</div>;
+		}),
+	};
+});
+
+const mockActions: RoomToolboxActionConfig[] = [
+	{ id: 'thread', icon: 'thread', title: 'Threads' as any, groups: ['channel'] },
+	{ id: 'members-list', icon: 'members', title: 'Members' as any, groups: ['channel'] },
+	{ id: 'discussions', icon: 'discussion', title: 'Discussions' as any, groups: ['channel'] },
+	{ id: 'files', icon: 'clip', title: 'Files' as any, groups: ['channel'] },
+	{ id: 'pinned-messages', icon: 'pin', title: 'Pinned Messages' as any, groups: ['channel'] },
+];
+
+const mockLayoutConfig = JSON.stringify({
+	maxVisibleNormal: 2,
+	items: [
+		{ id: 'thread', featured: true, order: 1 },
+		{ id: 'members-list', featured: false, order: 2 },
+		{ id: 'discussions', featured: false, order: 3 },
+	],
+});
 
 describe('RoomHeader', () => {
 	describe('Toolbox', () => {
@@ -62,4 +92,154 @@ describe('RoomHeader', () => {
 			expect(screen.getByText('Slotted Toolbox')).toBeInTheDocument();
 		});
 	});
+
+	describe('Room Toolbox Layout Engine', () => {
+		beforeAll(() => {
+			mockUseRealRoomToolbox.value = true;
+		});
+
+		afterAll(() => {
+			mockUseRealRoomToolbox.value = false;
+		});
+
+		const renderWithLayout = (
+			room = mockedRoom,
+			layoutContextValue?: Partial<LayoutContextValue>,
+			settings = {
+				Accounts_AllowFeaturePreview: true,
+				Room_Toolbox_Layout: mockLayoutConfig,
+			},
+			featuresPreview = [{ name: 'roomToolboxLayout', value: true }],
+		) => {
+			const mockLayoutContextValue: LayoutContextValue = {
+				isEmbedded: false,
+				showTopNavbarEmbeddedLayout: false,
+				isTablet: false,
+				isMobile: false,
+				roomToolboxExpanded: true,
+				navbar: { searchExpanded: false },
+				sidebar: {
+					overlayed: false,
+					setOverlayed: () => undefined,
+					isCollapsed: false,
+					shouldToggle: false,
+					toggle: () => undefined,
+					collapse: () => undefined,
+					expand: () => undefined,
+					close: () => undefined,
+				},
+				sidePanel: {
+					displaySidePanel: true,
+					closeSidePanel: () => undefined,
+					openSidePanel: () => undefined,
+				},
+				size: { sidebar: '240px', contextualBar: '380px' },
+				contextualBarPosition: 'relative',
+				contextualBarExpanded: false,
+				hiddenActions: {
+					roomToolbox: [],
+					messageToolbox: [],
+					composerToolbox: [],
+					userToolbox: [],
+				},
+				...layoutContextValue,
+			};
+
+			const mockToolboxValue = {
+				actions: mockActions,
+				openTab: () => undefined,
+				closeTab: () => undefined,
+			};
+
+			const appRootWithSettings = mockAppRoot()
+				.withSetting('Accounts_AllowFeaturePreview', settings.Accounts_AllowFeaturePreview)
+				.withSetting('Room_Toolbox_Layout', settings.Room_Toolbox_Layout)
+				.withUserPreference('featuresPreview', featuresPreview)
+				.withRoom(room)
+				.wrap((children) => <FakeRoomProvider roomOverrides={room}>{children}</FakeRoomProvider>)
+				.build();
+
+			return render(
+				<LayoutContext.Provider value={mockLayoutContextValue}>
+					<RoomToolboxContext.Provider value={mockToolboxValue}>
+						<RoomHeader room={room} slots={{}} />
+					</RoomToolboxContext.Provider>
+				</LayoutContext.Provider>,
+				{ wrapper: appRootWithSettings },
+			);
+		};
+
+		const roomScenarios = [
+			{ type: 'c', name: 'public-channel', title: 'Public Channel' },
+			{ type: 'p', name: 'private-group', title: 'Private Group' },
+			{ type: 'd', name: 'direct-message', title: 'Direct Message' },
+		] as const;
+
+		roomScenarios.forEach(({ type, name, title }) => {
+			describe(`Room Type: ${title}`, () => {
+				const testRoom = createFakeRoom({
+					prid: undefined,
+					t: type,
+					name,
+					fname: name,
+				});
+
+				it('should respect custom featured and visible actions layout and send remaining normal actions to options dropdown', () => {
+					renderWithLayout(testRoom);
+
+					expect(screen.getByTitle('Threads')).toBeInTheDocument();
+					expect(screen.getByTitle('Members')).toBeInTheDocument();
+					expect(screen.getByTitle('Discussions')).toBeInTheDocument();
+					expect(screen.queryByTitle('Files')).not.toBeInTheDocument();
+					expect(screen.getByTitle('Options')).toBeInTheDocument();
+				});
+
+				it('should collapse normal actions into kebab menu when roomToolboxExpanded is false (mobile viewport)', () => {
+					renderWithLayout(testRoom, { roomToolboxExpanded: false });
+
+					expect(screen.getByTitle('Threads')).toBeInTheDocument();
+					expect(screen.queryByTitle('Members')).not.toBeInTheDocument();
+					expect(screen.queryByTitle('Discussions')).not.toBeInTheDocument();
+					expect(screen.queryByTitle('Files')).not.toBeInTheDocument();
+					expect(screen.getByTitle('Options')).toBeInTheDocument();
+				});
+
+				describe('Soft Fallbacks', () => {
+					it('should fallback to legacy behavior if feature preview is disabled', () => {
+						renderWithLayout(testRoom, undefined, undefined, [{ name: 'roomToolboxLayout', value: false }]);
+
+						expect(screen.getByTitle('Threads')).toBeInTheDocument();
+						expect(screen.getByTitle('Members')).toBeInTheDocument();
+						expect(screen.getByTitle('Discussions')).toBeInTheDocument();
+						expect(screen.getByTitle('Files')).toBeInTheDocument();
+						expect(screen.getByTitle('Pinned Messages')).toBeInTheDocument();
+						expect(screen.queryByTitle('Options')).not.toBeInTheDocument();
+					});
+
+					it('should fallback to legacy behavior if layout configuration is malformed JSON', () => {
+						renderWithLayout(testRoom, undefined, {
+							Accounts_AllowFeaturePreview: true,
+							Room_Toolbox_Layout: '{ invalid json }',
+						});
+
+						expect(screen.getByTitle('Threads')).toBeInTheDocument();
+						expect(screen.getByTitle('Members')).toBeInTheDocument();
+						expect(screen.getByTitle('Discussions')).toBeInTheDocument();
+						expect(screen.getByTitle('Files')).toBeInTheDocument();
+						expect(screen.getByTitle('Pinned Messages')).toBeInTheDocument();
+						expect(screen.queryByTitle('Options')).not.toBeInTheDocument();
+					});
+				});
+
+				describe('Accessibility (a11y)', () => {
+					it('should not have any accessibility violations', async () => {
+						const { container } = renderWithLayout(testRoom);
+
+						const results = await axe(container);
+						expect(results).toHaveNoViolations();
+					});
+				});
+			});
+		});
+	});
 });
diff --git a/apps/meteor/client/views/room/Header/RoomToolbox/hooks/processRoomActions.ts b/apps/meteor/client/views/room/Header/RoomToolbox/hooks/processRoomActions.ts
index da6dade3a221f..d776820a2cb97 100644
--- a/apps/meteor/client/views/room/Header/RoomToolbox/hooks/processRoomActions.ts
+++ b/apps/meteor/client/views/room/Header/RoomToolbox/hooks/processRoomActions.ts
@@ -24,7 +24,7 @@ export const processRoomActions = (actionsBase: RoomToolboxBaseAction[], config:
 	const appActions = actionsBase.filter((a) => a.type === 'apps');
 	const nonAppActions = actionsBase.filter((a) => a.type !== 'apps');
 
-	if (!config?.items || config.items.length === 0) {
+	if (!config) {
 		const hiddenActions: RoomToolboxHiddenSection[] = [];
 		if (appActions.length > 0) {
 			hiddenActions.push({ id: 'apps', items: appActions });
@@ -36,7 +36,7 @@ export const processRoomActions = (actionsBase: RoomToolboxBaseAction[], config:
 		};
 	}
 
-	const itemMap = new Map(config.items.map((item) => [item.id, item]));
+	const itemMap = new Map((config.items || []).map((item) => [item.id, item]));
 
 	const [featuredWithOrder, normalWithOrder] = nonAppActions.reduce<
 		[{ action: RoomToolboxBaseAction; order: number }[], { action: RoomToolboxBaseAction; order: number }[]]
diff --git a/apps/meteor/client/views/room/Header/RoomToolbox/hooks/useRoomToolboxActions.ts b/apps/meteor/client/views/room/Header/RoomToolbox/hooks/useRoomToolboxActions.ts
index af9ef68bf1b60..61394dfd54574 100644
--- a/apps/meteor/client/views/room/Header/RoomToolbox/hooks/useRoomToolboxActions.ts
+++ b/apps/meteor/client/views/room/Header/RoomToolbox/hooks/useRoomToolboxActions.ts
@@ -87,7 +87,10 @@ export const useRoomToolboxActions = ({ actions, openTab }: Pick<RoomToolboxCont
 		const typedVisible = engineVisible as RoomToolboxActionConfig[];
 
 		if (!roomToolboxExpanded) {
-			const orderedOverflowActions = [...typedVisible, ...engineSections.flatMap((section) => section.items as RoomToolboxActionConfig[])];
+			const orderedOverflowActions = [
+				...typedVisible,
+				...engineSections.flatMap((section) => section.items as RoomToolboxActionConfig[]),
+			].filter((item) => !item.disabled);
 
 			const sectionsMap = new Map<string, MenuSection>();
 			for (const item of orderedOverflowActions) {
@@ -109,11 +112,15 @@ export const useRoomToolboxActions = ({ actions, openTab }: Pick<RoomToolboxCont
 			return { featuredActions: typedFeatured, visibleActions: [], hiddenActions };
 		}
 
-		const hiddenActions = engineSections.map((section) => ({
-			id: section.id,
-			title: section.id === 'apps' ? t('Apps') : '',
-			items: (section.items as RoomToolboxActionConfig[]).map((item) => actionToMenuItem(item, openTab, t)),
-		}));
+		const hiddenActions = engineSections
+			.map((section) => ({
+				id: section.id,
+				title: section.id === 'apps' ? t('Apps') : '',
+				items: (section.items as RoomToolboxActionConfig[])
+					.filter((item) => !item.disabled)
+					.map((item) => actionToMenuItem(item, openTab, t)),
+			}))
+			.filter((section) => section.items.length > 0);
 
 		return { featuredActions: typedFeatured, visibleActions: typedVisible, hiddenActions };
 	}