diff --git a/src/app-layout/__tests__/app-layout-navigation.test.tsx b/src/app-layout/__tests__/app-layout-navigation.test.tsx
index 470d5c2880..cbba909c0f 100644
--- a/src/app-layout/__tests__/app-layout-navigation.test.tsx
+++ b/src/app-layout/__tests__/app-layout-navigation.test.tsx
@@ -63,6 +63,15 @@ describeEachAppLayout({ themes: ['refresh-toolbar'], sizes: ['desktop'] }, () =>
     expect(wrapper.findOpenNavigationPanel()).toBeTruthy();
   });
 
+  test('close button does not open navigation when already closed', () => {
+    const { wrapper } = renderComponent(<AppLayout navigation={<>Mock Navigation</>} />);
+    expect(wrapper.findOpenNavigationPanel()).toBeTruthy();
+    wrapper.findNavigationToggle().click();
+    expect(wrapper.findOpenNavigationPanel()).toBeFalsy();
+    wrapper.findNavigationClose().click();
+    expect(wrapper.findOpenNavigationPanel()).toBeFalsy();
+  });
+
   test(`Sets aria-expanded=false on toggle when navigation is closed`, () => {
     const { wrapper } = renderComponent(
       <AppLayout navigation={<>Mock Navigation</>} navigationOpen={false} content={<>Content</>} />
diff --git a/src/app-layout/__tests__/navigation-collapsed.test.tsx b/src/app-layout/__tests__/navigation-collapsed.test.tsx
index 45729689ee..077278d37e 100644
--- a/src/app-layout/__tests__/navigation-collapsed.test.tsx
+++ b/src/app-layout/__tests__/navigation-collapsed.test.tsx
@@ -52,6 +52,17 @@ describeEachAppLayout({ themes: ['refresh-toolbar'], sizes: ['desktop'] }, () =>
       const closeButton = wrapper.findNavigationClose().getElement();
       expect(closeButton.querySelector(`.${iconStyles['name-angle-left']}`)).not.toBeNull();
     });
+
+    test('close button toggles navigation open and closed when collapsible', () => {
+      const { wrapper } = renderComponent(
+        <AppLayout navigationCloseBehavior="collapse" navigation={<>Nav content</>} />
+      );
+      expect(wrapper.findOpenNavigationPanel()).toBeTruthy();
+      wrapper.findNavigationClose().click();
+      expect(wrapper.findOpenNavigationPanel()).toBeFalsy();
+      wrapper.findNavigationClose().click();
+      expect(wrapper.findOpenNavigationPanel()).toBeTruthy();
+    });
   });
 
   describe('aria-expanded', () => {
diff --git a/src/app-layout/visual-refresh-toolbar/navigation/index.tsx b/src/app-layout/visual-refresh-toolbar/navigation/index.tsx
index 759387fc12..3150d0a41b 100644
--- a/src/app-layout/visual-refresh-toolbar/navigation/index.tsx
+++ b/src/app-layout/visual-refresh-toolbar/navigation/index.tsx
@@ -91,7 +91,7 @@ export function AppLayoutNavigationImplementation({
             }
             ariaExpanded={navigationCollapsible && !isMobile ? navigationOpen : undefined}
             iconName={navigationCollapsed ? 'angle-right' : isMobile ? 'close' : 'angle-left'}
-            onClick={() => onNavigationToggle(!navigationOpen)}
+            onClick={() => onNavigationToggle(navigationCollapsible ? !navigationOpen : false)}
             variant="icon"
             formAction="none"
             className={testutilStyles['navigation-close']}