diff --git a/packages/eui/src/components/flyout/flyout.component.tsx b/packages/eui/src/components/flyout/flyout.component.tsx
index b2331e3c2a4..c4300b8878c 100644
--- a/packages/eui/src/components/flyout/flyout.component.tsx
+++ b/packages/eui/src/components/flyout/flyout.component.tsx
@@ -611,6 +611,15 @@ export const EuiFlyoutComponent = forwardRef(
       return _titleId || generatedMenuId;
     }, [hasMenu, _titleId, generatedMenuId]);
 
+    // If the flyout level is LEVEL_MAIN, the title should be hidden by default
+    const flyoutMenuHideTitle = useMemo(() => {
+      if (!hasMenu) return undefined;
+      if (_flyoutMenuProps?.hideTitle !== undefined) {
+        return _flyoutMenuProps.hideTitle;
+      }
+      return currentSession?.mainFlyoutId === flyoutId;
+    }, [hasMenu, _flyoutMenuProps, currentSession, flyoutId]);
+
     const ariaLabelledBy = useMemo(() => {
       if (flyoutMenuId) {
         return classnames(flyoutMenuId, _ariaLabelledBy);
@@ -700,7 +709,11 @@ export const EuiFlyoutComponent = forwardRef(
               />
             )}
             {_flyoutMenuProps && (
-              <EuiFlyoutMenu {...flyoutMenuProps} titleId={flyoutMenuId} />
+              <EuiFlyoutMenu
+                {...flyoutMenuProps}
+                hideTitle={flyoutMenuHideTitle}
+                titleId={flyoutMenuId}
+              />
             )}
             {resizable && (
               <EuiFlyoutResizeButton
diff --git a/packages/eui/src/components/flyout/flyout_menu.stories.tsx b/packages/eui/src/components/flyout/flyout_menu.stories.tsx
index 44e571933d2..b8e631fd933 100644
--- a/packages/eui/src/components/flyout/flyout_menu.stories.tsx
+++ b/packages/eui/src/components/flyout/flyout_menu.stories.tsx
@@ -16,6 +16,7 @@ import { EuiText } from '../text';
 import { EuiFlyout } from './flyout';
 import { EuiFlyoutBody } from './flyout_body';
 import { EuiFlyoutMenu, EuiFlyoutMenuProps } from './flyout_menu';
+import { EuiFlyoutHeader } from './flyout_header';
 
 interface Args extends EuiFlyoutMenuProps {
   showCustomActions: boolean;
@@ -26,6 +27,7 @@ const meta: Meta<Args> = {
   title: 'Layout/EuiFlyout/EuiFlyoutMenu',
   component: EuiFlyoutMenu,
   argTypes: {
+    hideTitle: { control: 'boolean' },
     showBackButton: { control: 'boolean' },
     showCustomActions: { control: 'boolean' },
     'aria-label': { table: { disable: true } },
@@ -38,6 +40,7 @@ const meta: Meta<Args> = {
     showBackButton: true,
     showCustomActions: true,
     showHistoryItems: true,
+    hideTitle: true,
   },
 };
 
@@ -45,6 +48,7 @@ export default meta;
 
 const MenuBarFlyout = (args: Args) => {
   const {
+    hideTitle,
     hideCloseButton,
     showBackButton,
     showCustomActions,
@@ -80,6 +84,8 @@ const MenuBarFlyout = (args: Args) => {
     'aria-label': `${iconType} action`,
   }));
 
+  const titleId = 'menu-bar-example-main-title';
+
   return (
     <>
       <EuiButton onClick={openFlyout} disabled={isFlyoutOpen}>
@@ -94,8 +100,11 @@ const MenuBarFlyout = (args: Args) => {
           type="overlay"
           outsideClickCloses={false}
           ownFocus
+          aria-labelledby={titleId}
           flyoutMenuProps={{
             title: 'Flyout title',
+            titleId,
+            hideTitle,
             hideCloseButton,
             showBackButton,
             backButtonProps,
@@ -103,6 +112,13 @@ const MenuBarFlyout = (args: Args) => {
             customActions: showCustomActions ? customActions : undefined,
           }}
         >
+          {hideTitle && (
+            <EuiFlyoutHeader hasBorder>
+              <EuiText>
+                <h2 id={titleId}>Simple flyout header</h2>
+              </EuiText>
+            </EuiFlyoutHeader>
+          )}
           <EuiFlyoutBody>
             <EuiText>
               <p>Simple flyout content.</p>
diff --git a/packages/eui/src/components/flyout/flyout_menu.styles.ts b/packages/eui/src/components/flyout/flyout_menu.styles.ts
index d3ae142bf39..af73cfd659f 100644
--- a/packages/eui/src/components/flyout/flyout_menu.styles.ts
+++ b/packages/eui/src/components/flyout/flyout_menu.styles.ts
@@ -8,6 +8,7 @@
 
 import { css } from '@emotion/react';
 import { UseEuiTheme } from '../../services';
+import { euiScreenReaderOnly } from '../accessibility';
 
 export const euiFlyoutMenuStyles = (euiThemeContext: UseEuiTheme) => {
   const { euiTheme } = euiThemeContext;
@@ -31,5 +32,8 @@ export const euiFlyoutMenuStyles = (euiThemeContext: UseEuiTheme) => {
     euiFlyoutMenu__actions: css`
       block-size: calc(${euiTheme.size.m} * 1.8);
     `,
+    euiFlyoutMenu__hiddenTitle: css`
+      ${euiScreenReaderOnly()}
+    `,
   };
 };
diff --git a/packages/eui/src/components/flyout/flyout_menu.test.tsx b/packages/eui/src/components/flyout/flyout_menu.test.tsx
new file mode 100644
index 00000000000..f63652f2146
--- /dev/null
+++ b/packages/eui/src/components/flyout/flyout_menu.test.tsx
@@ -0,0 +1,289 @@
+/*
+ * Copyright Elasticsearch B.V. and/or licensed to Elasticsearch B.V. under one
+ * or more contributor license agreements. Licensed under the Elastic License
+ * 2.0 and the Server Side Public License, v 1; you may not use this file except
+ * in compliance with, at your election, the Elastic License 2.0 or the Server
+ * Side Public License, v 1.
+ */
+
+import React from 'react';
+import { render, screen } from '../../test/rtl';
+import { requiredProps } from '../../test';
+
+import { EuiFlyoutMenu } from './flyout_menu';
+import { EuiFlyoutMenuContext } from './flyout_menu_context';
+
+describe('EuiFlyoutMenu', () => {
+  const onClose = jest.fn();
+
+  beforeEach(() => {
+    jest.clearAllMocks();
+  });
+
+  const renderWithContext = (ui: React.ReactElement) => {
+    return render(
+      <EuiFlyoutMenuContext.Provider value={{ onClose }}>
+        {ui}
+      </EuiFlyoutMenuContext.Provider>
+    );
+  };
+
+  describe('basic rendering', () => {
+    it('renders with title', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu {...requiredProps} title="Test Title" />
+      );
+
+      expect(container.querySelector('.euiFlyoutMenu')).toBeInTheDocument();
+      expect(screen.getByText('Test Title')).toBeInTheDocument();
+    });
+
+    it('renders without title', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu {...requiredProps} />
+      );
+
+      expect(container.querySelector('.euiFlyoutMenu')).toBeInTheDocument();
+    });
+
+    it('renders with custom titleId', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu
+          {...requiredProps}
+          title="Custom Title"
+          titleId="my-custom-id"
+        />
+      );
+
+      const titleElement = container.querySelector('#my-custom-id');
+      expect(titleElement).toBeInTheDocument();
+      expect(titleElement?.textContent).toBe('Custom Title');
+    });
+  });
+
+  describe('hideTitle prop', () => {
+    it('shows title by default when hideTitle is not specified', () => {
+      const { getByText } = renderWithContext(
+        <EuiFlyoutMenu title="Visible Title" />
+      );
+
+      const title = getByText('Visible Title');
+      expect(title).toBeInTheDocument();
+      expect(title).toBeVisible();
+    });
+
+    it('applies screen reader only styles when hideTitle is true', () => {
+      const { container, getByText } = renderWithContext(
+        <EuiFlyoutMenu
+          title="Hidden Title"
+          titleId="test-title-id"
+          hideTitle={true}
+        />
+      );
+
+      const titleContainer = container.querySelector('#test-title-id');
+      expect(titleContainer).toBeInTheDocument();
+
+      const titleText = getByText('Hidden Title');
+      expect(titleText).toBeInTheDocument();
+      // The title should have the hiddenTitle CSS class applied
+      // We can't test visibility directly in JSDOM as CSS-in-JS isn't fully evaluated
+      expect(titleText.className).toContain('euiFlyoutMenu__hiddenTitle');
+    });
+
+    it('shows title when hideTitle is false', () => {
+      const { getByText } = renderWithContext(
+        <EuiFlyoutMenu title="Visible Title" hideTitle={false} />
+      );
+
+      const title = getByText('Visible Title');
+      expect(title).toBeVisible();
+    });
+  });
+
+  describe('close button', () => {
+    it('renders close button by default', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" />
+      );
+
+      expect(
+        container.querySelector('[data-test-subj="euiFlyoutCloseButton"]')
+      ).toBeInTheDocument();
+    });
+
+    it('hides close button when hideCloseButton is true', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" hideCloseButton={true} />
+      );
+
+      expect(
+        container.querySelector('[data-test-subj="euiFlyoutCloseButton"]')
+      ).not.toBeInTheDocument();
+    });
+
+    it('calls onClose when close button is clicked', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" />
+      );
+
+      const closeButton = container.querySelector(
+        '[data-test-subj="euiFlyoutCloseButton"]'
+      );
+      closeButton?.dispatchEvent(new MouseEvent('click', { bubbles: true }));
+
+      expect(onClose).toHaveBeenCalledTimes(1);
+    });
+  });
+
+  describe('back button', () => {
+    it('does not render back button by default', () => {
+      const { queryByText } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" />
+      );
+
+      expect(queryByText('Back')).not.toBeInTheDocument();
+    });
+
+    it('renders back button when showBackButton is true', () => {
+      const { getByText } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" showBackButton={true} />
+      );
+
+      expect(getByText('Back')).toBeInTheDocument();
+    });
+
+    it('calls backButtonProps.onClick when back button is clicked', () => {
+      const handleBack = jest.fn();
+      const { getByText } = renderWithContext(
+        <EuiFlyoutMenu
+          title="Test Title"
+          showBackButton={true}
+          backButtonProps={{ onClick: handleBack }}
+        />
+      );
+
+      getByText('Back').click();
+      expect(handleBack).toHaveBeenCalledTimes(1);
+    });
+  });
+
+  describe('history items', () => {
+    const historyItems = [
+      { title: 'History 1', onClick: jest.fn() },
+      { title: 'History 2', onClick: jest.fn() },
+    ];
+
+    it('does not render history popover when historyItems is empty', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" historyItems={[]} />
+      );
+
+      expect(
+        container.querySelector('[aria-label="History"]')
+      ).not.toBeInTheDocument();
+    });
+
+    it('renders history popover when historyItems are provided', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" historyItems={historyItems} />
+      );
+
+      expect(
+        container.querySelector('[aria-label="History"]')
+      ).toBeInTheDocument();
+    });
+  });
+
+  describe('custom actions', () => {
+    const customActions = [
+      {
+        iconType: 'gear',
+        onClick: jest.fn(),
+        'aria-label': 'Settings',
+      },
+      {
+        iconType: 'share',
+        onClick: jest.fn(),
+        'aria-label': 'Share',
+      },
+    ];
+
+    it('does not render custom actions when not provided', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" />
+      );
+
+      expect(container.querySelectorAll('.euiButtonIcon').length).toBe(1); // Only close button
+    });
+
+    it('renders custom action buttons', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" customActions={customActions} />
+      );
+
+      const buttons = container.querySelectorAll('.euiButtonIcon');
+      // Should have 2 custom actions + 1 close button = 3 total
+      expect(buttons.length).toBeGreaterThanOrEqual(2);
+    });
+
+    it('calls onClick when custom action is clicked', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test Title" customActions={customActions} />
+      );
+
+      const settingsButton = container.querySelector('[aria-label="Settings"]');
+      settingsButton?.dispatchEvent(new MouseEvent('click', { bubbles: true }));
+
+      expect(customActions[0].onClick).toHaveBeenCalledTimes(1);
+    });
+  });
+
+  describe('accessibility', () => {
+    it('title is accessible even when hidden', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu
+          title="Screen Reader Title"
+          titleId="sr-title"
+          hideTitle={true}
+        />
+      );
+
+      const title = container.querySelector('#sr-title');
+      expect(title).toBeInTheDocument();
+      expect(title?.textContent).toBe('Screen Reader Title');
+      // The title should still be accessible to screen readers
+    });
+
+    it('provides aria-label for back button', () => {
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu
+          title="Test"
+          showBackButton={true}
+          backButtonProps={{
+            onClick: jest.fn(),
+            'aria-label': 'Go back',
+          }}
+        />
+      );
+
+      const backButton = container.querySelector(
+        'button[aria-label="Go back"]'
+      );
+      expect(backButton).toBeInTheDocument();
+    });
+
+    it('provides aria-labels for custom actions', () => {
+      const customActions = [
+        { iconType: 'gear', onClick: jest.fn(), 'aria-label': 'Settings' },
+      ];
+
+      const { container } = renderWithContext(
+        <EuiFlyoutMenu title="Test" customActions={customActions} />
+      );
+
+      const settingsButton = container.querySelector('[aria-label="Settings"]');
+      expect(settingsButton).toBeInTheDocument();
+    });
+  });
+});
diff --git a/packages/eui/src/components/flyout/flyout_menu.tsx b/packages/eui/src/components/flyout/flyout_menu.tsx
index ae735158385..1330d789724 100644
--- a/packages/eui/src/components/flyout/flyout_menu.tsx
+++ b/packages/eui/src/components/flyout/flyout_menu.tsx
@@ -47,7 +47,7 @@ export interface EuiFlyoutHistoryItem {
 }
 
 /**
- * Custom action item for the flyout menu header
+ * Custom action item for the flyout menu component
  */
 export interface EuiFlyoutMenuCustomAction {
   /**
@@ -75,26 +75,29 @@ export type EuiFlyoutMenuProps = CommonProps &
      * ```jsx
      * <EuiFlyout
      *   aria-labelledby="myMenuTitleId"
+     *   flyoutMenuProps={{ title: 'Menu title', titleId: 'myMenuTitleId' }
      * >
-     *   <EuiFlyoutMenu
-     *     titleId="myMenuTitleId"
-     *     title="Menu title"
-     *   />
+     *  ...
      * </EuiFlyout>
      * ```
      */
     titleId?: string;
     /**
-     * Title for the menu header
+     * Title for the menu component. In a managed flyout context, the title is used to indicate the flyout session for history navigation.
      */
     title?: React.ReactNode;
     /**
-     * Hides the close button in the menu header
+     * Hides the title in the `EuiFlyoutMenu`. This is useful when the title is already shown in an `EuiFlyoutHeader`.
+     * @default true for main flyout in a managed flyout session; false otherwise
+     */
+    hideTitle?: boolean;
+    /**
+     * Hides the close button in the menu component
      * @default false
      */
     hideCloseButton?: boolean;
     /**
-     * Shows a back button in the menu header
+     * Shows a back button in the menu component
      * @default false
      */
     showBackButton?: boolean;
@@ -107,7 +110,7 @@ export type EuiFlyoutMenuProps = CommonProps &
      */
     historyItems?: EuiFlyoutHistoryItem[];
     /**
-     * List of custom action items for the menu header
+     * List of custom action items for the menu component
      */
     customActions?: EuiFlyoutMenuCustomAction[];
   };
@@ -172,9 +175,10 @@ const HistoryPopover: React.FC<{
  * @private
  */
 export const EuiFlyoutMenu: FunctionComponent<EuiFlyoutMenuProps> = ({
-  titleId,
   className,
   title,
+  titleId,
+  hideTitle,
   hideCloseButton,
   historyItems = [],
   showBackButton,
@@ -191,7 +195,7 @@ export const EuiFlyoutMenu: FunctionComponent<EuiFlyoutMenuProps> = ({
   if (title) {
     titleNode = (
       <EuiTitle size="xxs" id={titleId}>
-        <h3>{title}</h3>
+        <h3 css={hideTitle && styles.euiFlyoutMenu__hiddenTitle}>{title}</h3>
       </EuiTitle>
     );
   }
diff --git a/packages/eui/src/components/flyout/manager/flyout_managed.test.tsx b/packages/eui/src/components/flyout/manager/flyout_managed.test.tsx
index be678d38556..85d7648bab2 100644
--- a/packages/eui/src/components/flyout/manager/flyout_managed.test.tsx
+++ b/packages/eui/src/components/flyout/manager/flyout_managed.test.tsx
@@ -277,6 +277,96 @@ describe('EuiManagedFlyout', () => {
     });
   });
 
+  describe('hideTitle prop handling', () => {
+    it('passes hideTitle prop through flyoutMenuProps when explicitly set to true', () => {
+      const { getByTestSubject } = renderInProvider(
+        <EuiManagedFlyout
+          id="test-flyout"
+          level={LEVEL_MAIN}
+          onClose={() => {}}
+          flyoutMenuProps={{
+            title: 'Test Title',
+            hideTitle: true,
+          }}
+        />
+      );
+
+      const flyout = getByTestSubject('managed-flyout');
+      expect(flyout).toBeInTheDocument();
+      // The hideTitle prop should be passed through to the base component
+    });
+
+    it('passes hideTitle prop through flyoutMenuProps when explicitly set to false', () => {
+      const { getByTestSubject } = renderInProvider(
+        <EuiManagedFlyout
+          id="test-flyout"
+          level={LEVEL_MAIN}
+          onClose={() => {}}
+          flyoutMenuProps={{
+            title: 'Test Title',
+            hideTitle: false,
+          }}
+        />
+      );
+
+      const flyout = getByTestSubject('managed-flyout');
+      expect(flyout).toBeInTheDocument();
+      // The hideTitle prop should be passed through to the base component
+    });
+
+    it('merges hideTitle with other flyoutMenuProps correctly', () => {
+      const { getByTestSubject } = renderInProvider(
+        <EuiManagedFlyout
+          id="test-flyout"
+          level={LEVEL_MAIN}
+          onClose={() => {}}
+          flyoutMenuProps={{
+            title: 'Test Title',
+            hideTitle: true,
+            hideCloseButton: false,
+          }}
+        />
+      );
+
+      const flyout = getByTestSubject('managed-flyout');
+      expect(flyout).toBeInTheDocument();
+    });
+
+    it('does not include hideTitle when not specified for main flyout', () => {
+      const { getByTestSubject } = renderInProvider(
+        <EuiManagedFlyout
+          id="test-flyout"
+          level={LEVEL_MAIN}
+          onClose={() => {}}
+          flyoutMenuProps={{
+            title: 'Test Title',
+            // hideTitle not specified - will be auto-determined by base component
+          }}
+        />
+      );
+
+      const flyout = getByTestSubject('managed-flyout');
+      expect(flyout).toBeInTheDocument();
+    });
+
+    it('does not include hideTitle when not specified for child flyout', () => {
+      const { getByTestSubject } = renderInProvider(
+        <EuiManagedFlyout
+          id="child-flyout"
+          level={LEVEL_CHILD}
+          onClose={() => {}}
+          flyoutMenuProps={{
+            title: 'Child Title',
+            // hideTitle not specified - will be auto-determined by base component
+          }}
+        />
+      );
+
+      const flyout = getByTestSubject('managed-flyout');
+      expect(flyout).toBeInTheDocument();
+    });
+  });
+
   describe('size handling', () => {
     it('defaults main flyout size to "m" when no size is provided', () => {
       // Import the real validation function to test the actual behavior
diff --git a/packages/eui/src/components/flyout/manager/flyout_managed.tsx b/packages/eui/src/components/flyout/manager/flyout_managed.tsx
index 7b5d4580d8c..090fe751e4c 100644
--- a/packages/eui/src/components/flyout/manager/flyout_managed.tsx
+++ b/packages/eui/src/components/flyout/manager/flyout_managed.tsx
@@ -5,8 +5,10 @@
  * in compliance with, at your election, the Elastic License 2.0 or the Server
  * Side Public License, v 1.
  */
+
 import React, { useEffect, useMemo, useRef } from 'react';
 import { useEuiMemoizedStyles } from '../../../services';
+import { useEuiI18n } from '../../i18n';
 import { useResizeObserver } from '../../observer/resize_observer';
 import {
   EuiFlyoutComponent,
@@ -38,7 +40,6 @@ import type { EuiFlyoutLevel } from './types';
 import {
   createValidationErrorMessage,
   isNamedSize,
-  validateFlyoutTitle,
   validateManagedFlyoutSize,
   validateSizeCombination,
 } from './validation';
@@ -119,11 +120,23 @@ export const EuiManagedFlyout = ({
     }
   }
 
-  // Validate title
-  const title = _flyoutMenuProps?.title || props['aria-label'];
-  const titleError = validateFlyoutTitle(title, flyoutId, level);
-  if (titleError) {
-    throw new Error(createValidationErrorMessage(titleError));
+  const defaultTitle = useEuiI18n(
+    'euiFlyoutManaged.defaultTitle',
+    'Unknown Flyout'
+  );
+
+  // Set title from flyoutMenuProps or aria-label
+  // TODO: allow aria-labelledby references to be used
+  let title = _flyoutMenuProps?.title || props['aria-label'];
+  if (
+    process.env.NODE_ENV === 'development' &&
+    level === LEVEL_MAIN &&
+    !title
+  ) {
+    console.warn(
+      `Managed flyout "${flyoutId}" requires a title, which can be provided through 'flyoutMenuProps.title' or 'aria-label'. Using default title: "${defaultTitle}"`
+    );
+    title = defaultTitle;
   }
 
   const isActive = useIsFlyoutActive(flyoutId);
diff --git a/packages/eui/src/components/flyout/manager/flyout_manager.stories.tsx b/packages/eui/src/components/flyout/manager/flyout_manager.stories.tsx
index 7cf1641986f..1e722779576 100644
--- a/packages/eui/src/components/flyout/manager/flyout_manager.stories.tsx
+++ b/packages/eui/src/components/flyout/manager/flyout_manager.stories.tsx
@@ -19,6 +19,7 @@ import { EuiFlyoutBody } from '../flyout_body';
 import { EuiFlyoutFooter } from '../flyout_footer';
 import { EuiFlyoutChild, EuiFlyoutChildProps } from './flyout_child';
 import { useFlyoutLayoutMode } from './hooks';
+import { EuiFlyoutHeader } from '../flyout_header';
 
 type EuiFlyoutChildActualProps = Pick<
   EuiFlyoutChildProps,
@@ -226,6 +227,13 @@ const StatefulFlyout: React.FC<FlyoutChildStoryArgs> = ({
           {...args}
           onClose={closeMain}
         >
+          <EuiFlyoutHeader>
+            <EuiText>
+              <h2 id="flyout-manager-playground-main-header">
+                Main Flyout Menu ({mainSize})
+              </h2>
+            </EuiText>
+          </EuiFlyoutHeader>
           <EuiFlyoutBody>
             <EuiText>
               <p>This is the main flyout content.</p>
diff --git a/packages/eui/src/components/flyout/manager/flyout_sessions.stories.tsx b/packages/eui/src/components/flyout/manager/flyout_sessions.stories.tsx
index 163473f96d0..dafa9ee6856 100644
--- a/packages/eui/src/components/flyout/manager/flyout_sessions.stories.tsx
+++ b/packages/eui/src/components/flyout/manager/flyout_sessions.stories.tsx
@@ -170,6 +170,11 @@ const FlyoutSession: React.FC<FlyoutSessionProps> = (props) => {
           onActive={mainFlyoutOnActive}
           onClose={mainFlyoutOnClose}
         >
+          <EuiFlyoutHeader>
+            <EuiTitle size="m">
+              <h2 id={`mainFlyoutTitle-${title}`}>{title} - Main Flyout</h2>
+            </EuiTitle>
+          </EuiFlyoutHeader>
           <EuiFlyoutBody>
             <EuiText>
               <p>This is the content of {title}.</p>
@@ -206,7 +211,6 @@ const FlyoutSession: React.FC<FlyoutSessionProps> = (props) => {
             <EuiFlyout
               id={`childFlyout-${title}`}
               flyoutMenuProps={{ title: `${title} - Child` }}
-              aria-labelledby="childFlyoutTitle"
               size={childSize}
               maxWidth={childMaxWidth}
               onActive={childFlyoutOnActive}
@@ -623,6 +627,13 @@ const ExternalRootFlyout: React.FC<{ id: string }> = ({ id }) => {
           ownFocus={false}
           flyoutMenuProps={{ title: `${id} flyout` }}
         >
+          <EuiFlyoutHeader>
+            <EuiTitle size="m">
+              <h2 id={`externalRootFlyoutTitle-${id}`}>
+                {id} - External Root Flyout
+              </h2>
+            </EuiTitle>
+          </EuiFlyoutHeader>
           <EuiFlyoutBody>
             <EuiText>
               <p>
diff --git a/packages/eui/src/components/flyout/manager/validation.test.ts b/packages/eui/src/components/flyout/manager/validation.test.ts
index 55cb531c56c..4835b348112 100644
--- a/packages/eui/src/components/flyout/manager/validation.test.ts
+++ b/packages/eui/src/components/flyout/manager/validation.test.ts
@@ -12,7 +12,6 @@ import {
   validateSizeCombination,
   createValidationErrorMessage,
   FlyoutValidationError,
-  validateFlyoutTitle,
 } from './validation';
 
 describe('Flyout Size Validation', () => {
@@ -49,7 +48,7 @@ describe('Flyout Size Validation', () => {
       expect(error).toEqual({
         type: 'INVALID_SIZE_TYPE',
         message:
-          'Child flyouts must use named sizes (s, m, l, fill). Received: 100px',
+          'Child flyout test-id must use a named size (s, m, l, fill). Received: 100px',
         flyoutId: 'test-id',
         level: 'child',
         size: '100px',
@@ -57,26 +56,6 @@ describe('Flyout Size Validation', () => {
     });
   });
 
-  describe('validateFlyoutTitle', () => {
-    it('should return null for child flyouts without title', () => {
-      expect(validateFlyoutTitle(undefined, 'child-id', 'child')).toBeNull();
-    });
-
-    it('should return null for main flyouts with valid title', () => {
-      expect(validateFlyoutTitle('Main Title', 'main-id', 'main')).toBeNull();
-    });
-
-    it('should return error for empty string title', () => {
-      const error = validateFlyoutTitle('', 'test-id', 'main');
-      expect(error).toEqual({
-        type: 'INVALID_FLYOUT_MENU_TITLE',
-        message: `Managed flyouts require either a 'flyoutMenuProps.title' or an 'aria-label' to provide the flyout menu title.`,
-        flyoutId: 'test-id',
-        level: 'main',
-      });
-    });
-  });
-
   describe('validateSizeCombination', () => {
     it('should return null for valid combinations', () => {
       expect(validateSizeCombination('s', 'm')).toBeNull();
@@ -141,7 +120,7 @@ describe('Flyout Size Validation', () => {
       const error: FlyoutValidationError = {
         type: 'INVALID_SIZE_TYPE',
         message:
-          'Child flyouts must use named sizes (s, m, l, fill). Received: 100px',
+          'Child flyout test-id must use a named size (s, m, l, fill). Received: 100px',
         flyoutId: 'test-id',
         level: 'child',
         size: '100px',
@@ -149,7 +128,7 @@ describe('Flyout Size Validation', () => {
 
       const message = createValidationErrorMessage(error);
       expect(message).toBe(
-        'EuiFlyout validation error: Child flyouts must use named sizes (s, m, l, fill). Received: 100px'
+        'EuiFlyout validation error: Child flyout test-id must use a named size (s, m, l, fill). Received: 100px'
       );
       expect(consoleSpy).toHaveBeenCalledWith(error);
     });
@@ -184,14 +163,14 @@ describe('Flyout Size Validation', () => {
       const error: FlyoutValidationError = {
         type: 'INVALID_FLYOUT_MENU_TITLE',
         message:
-          "Managed flyouts require either a 'flyoutMenuProps.title' or an 'aria-label' to provide the flyout menu title.",
+          'Managed flyout "test-id" requires a title, which can be provided through \'aria-label\' or \'flyoutMenuProps.title\'. Using default title: "Unknown Flyout"',
         flyoutId: 'test-id',
         level: 'main',
       };
 
       const message = createValidationErrorMessage(error);
       expect(message).toBe(
-        "EuiFlyout validation error: Managed flyouts require either a 'flyoutMenuProps.title' or an 'aria-label' to provide the flyout menu title."
+        'EuiFlyout validation error: Managed flyout "test-id" requires a title, which can be provided through \'aria-label\' or \'flyoutMenuProps.title\'. Using default title: "Unknown Flyout"'
       );
       expect(consoleSpy).toHaveBeenCalledWith(error);
     });
diff --git a/packages/eui/src/components/flyout/manager/validation.ts b/packages/eui/src/components/flyout/manager/validation.ts
index caf784da2cf..0c50ef81871 100644
--- a/packages/eui/src/components/flyout/manager/validation.ts
+++ b/packages/eui/src/components/flyout/manager/validation.ts
@@ -8,8 +8,7 @@
 
 import { EuiFlyoutSize, FLYOUT_SIZES } from '../const';
 import { EuiFlyoutComponentProps } from '../flyout.component';
-import { EuiFlyoutMenuProps } from '../flyout_menu';
-import { LEVEL_CHILD, LEVEL_MAIN } from './const';
+import { LEVEL_CHILD } from './const';
 import { EuiFlyoutLevel } from './types';
 
 type FlyoutValidationErrorType =
@@ -46,7 +45,7 @@ export function validateManagedFlyoutSize(
     const namedSizes = FLYOUT_SIZES.join(', ');
     return {
       type: 'INVALID_SIZE_TYPE',
-      message: `Child flyouts must use named sizes (${namedSizes}). Received: ${size}`,
+      message: `Child flyout ${flyoutId} must use a named size (${namedSizes}). Received: ${size}`,
       flyoutId,
       level,
       size,
@@ -55,25 +54,6 @@ export function validateManagedFlyoutSize(
   return null;
 }
 
-/**
- * Validates that a title is provided
- */
-export function validateFlyoutTitle(
-  flyoutMenuTitle: EuiFlyoutMenuProps['title'] | undefined,
-  flyoutId: string,
-  level: EuiFlyoutLevel
-): FlyoutValidationError | null {
-  if (level === LEVEL_MAIN && !flyoutMenuTitle) {
-    return {
-      type: 'INVALID_FLYOUT_MENU_TITLE',
-      message: `Managed flyouts require either a 'flyoutMenuProps.title' or an 'aria-label' to provide the flyout menu title.`,
-      flyoutId,
-      level,
-    };
-  }
-  return null;
-}
-
 /**
  * Validates size combinations for parent-child flyouts
  */
diff --git a/packages/website/docs/components/containers/flyout/session-management.mdx b/packages/website/docs/components/containers/flyout/session-management.mdx
index bd3bed96bbc..1949d8166fb 100644
--- a/packages/website/docs/components/containers/flyout/session-management.mdx
+++ b/packages/website/docs/components/containers/flyout/session-management.mdx
@@ -39,8 +39,17 @@ export default () => {
         <EuiFlyout
           session="start"
           size="s"
+          aria-labelledby="welcomeHeading"
+          flyoutMenuProps={{ title: 'Flyout A' }}
           onClose={() => setIsOpenFlyoutA(false)}
         >
+          <EuiFlyoutHeader>
+            <EuiTitle>
+              <h2 id="welcomeHeading">
+                Welcome to the flyout session management journey!
+              </h2>
+            </EuiTitle>
+          </EuiFlyoutHeader>
           <EuiFlyoutBody>
             <EuiText>This is <strong>Flyout A</strong>. This flyout is rendered with the <EuiCode>{'session="start"'}</EuiCode> prop set which created a new flyout session and marks this flyout as main.</EuiText>
             <EuiSpacer />
@@ -56,12 +65,17 @@ export default () => {
         <EuiFlyout
           session="start"
           size="m"
-          aria-label="Flyout B - main"
-          flyoutMenuProps={{
-            title: <>Glad to meet you, {name || 'stranger'}!</>,
-          }}
+          aria-labelledby="flyoutBHeading"
+          flyoutMenuProps={{ title: 'Flyout B' }}
           onClose={() => setIsOpenFlyoutB(false)}
         >
+          <EuiFlyoutHeader>
+            <EuiTitle>
+              <h2 id="flyoutBHeading">
+                Glad to meet you, {name || 'stranger'}!
+              </h2>
+            </EuiTitle>
+          </EuiFlyoutHeader>
           <EuiFlyoutBody>
             <EuiText>
               This is <strong>Flyout B</strong>. This flyout is also rendered with the <EuiCode>{'session="start"'}</EuiCode> prop added which creates a <strong>second flyout session</strong> and marks this flyout as main in that session.
@@ -75,9 +89,8 @@ export default () => {
           </EuiFlyoutBody>
           {isOpenFlyoutBChild && (
             <EuiFlyout
-              session="inherit"
               size="s"
-              aria-label="Flyout B - child"
+              aria-label="Child of Flyout B"
               onClose={() => setIsOpenFlyoutBChild(false)}
             >
               <EuiFlyoutBody>
@@ -125,9 +138,18 @@ configuration will be handled automatically.
 
 ### Session title
 
-Flyout sessions within the managed system require a title that can be
-referenced in the history navigation features. Use the `title`
-field of the `flyoutMenuProps` to set the title of the flyout.
+Managed flyout sessions require a title that can be referenced in the history
+navigation features. Use the `title` field of the `flyoutMenuProps` to set the
+title of the flyout session. If `flyoutMenuProps` is omitted or a `title` field
+is not given in `flyoutMenuProps`, the manager will use the `aria-label`
+attribute of `EuiFlyout` as the source for the session's title. If no source
+for a title is given, a default title will be provided.
+
+:::info Note
+The `title` from `flyoutMenuProps` is hidden from the menu on main flyouts (which should use
+`EuiFlyoutHeader` for the visible heading) but is displayed in the menu of child flyouts.
+For main flyouts, the title is primarily used for history navigation.
+:::
 
 ```tsx
 {/* Render a new main flyout and create a flyout session */}
@@ -136,9 +158,17 @@ field of the `flyoutMenuProps` to set the title of the flyout.
   flyoutMenuProps={{
     title: 'My main flyout'
   }}
+  aria-labelledby="myFlyoutHeading"
 >
+  <EuiFlyoutHeader>
+    <EuiTitle>
+      <h2 id="myFlyoutHeading">
+        I'm the main flyout heading
+      </h2>
+    </EuiTitle>
+  </EuiFlyoutHeader>
   <EuiFlyoutBody>
-    I'm the main flyout
+    I'm the main flyout body
   </EuiFlyoutBody>
   <EuiFlyout
     session="inherit"
@@ -146,7 +176,10 @@ field of the `flyoutMenuProps` to set the title of the flyout.
       title: 'My child flyout'
     }}
   >
-    I'm the child flyout that belongs to the same session as the main flyout
+    {/* Render a child flyout contents. Notice the lack of the EuiFlyoutHeader component - the child flyout menu shows the title from flyoutMenuProps */}
+    <EuiFlyoutBody>
+      I'm the child flyout that belongs to the same session as the main flyout
+    </EuiFlyoutBody>
   </EuiFlyout>
 </EuiFlyout>
 ```