diff --git a/src/aria/combobox/BUILD.bazel b/src/aria/combobox/BUILD.bazel
index d39dc069bf79..62e074472d70 100644
--- a/src/aria/combobox/BUILD.bazel
+++ b/src/aria/combobox/BUILD.bazel
@@ -11,6 +11,7 @@ ng_project(
     deps = [
         "//:node_modules/@angular/core",
         "//src/aria/private",
+        "//src/cdk/a11y",
         "//src/cdk/bidi",
     ],
 )
diff --git a/src/aria/combobox/combobox-widget.ts b/src/aria/combobox/combobox-widget.ts
index 3f4636e68ab4..82f33082633a 100644
--- a/src/aria/combobox/combobox-widget.ts
+++ b/src/aria/combobox/combobox-widget.ts
@@ -6,7 +6,17 @@
  * found in the LICENSE file at https://angular.dev/license
  */
 
-import {Directive, ElementRef, inject, input, OnDestroy, OnInit, signal} from '@angular/core';
+import {
+  afterNextRender,
+  Directive,
+  ElementRef,
+  inject,
+  input,
+  OnDestroy,
+  OnInit,
+  signal,
+} from '@angular/core';
+import {_IdGenerator} from '@angular/cdk/a11y';
 import {COMBOBOX_POPUP} from './combobox-tokens';
 
 /**
@@ -28,6 +38,7 @@ export class ComboboxWidget implements OnInit, OnDestroy {
   /** The element that the popup widget is attached to. */
   private readonly _elementRef = inject<ElementRef<HTMLElement>>(ElementRef);
   private readonly _popup = inject(COMBOBOX_POPUP);
+  private readonly _idGenerator = inject(_IdGenerator);
 
   /** A reference to the popup widget element. */
   readonly element = this._elementRef.nativeElement;
@@ -54,6 +65,16 @@ export class ComboboxWidget implements OnInit, OnDestroy {
       attributes: true,
       attributeFilter: ['id'],
     });
+
+    afterNextRender(() => {
+      // Imperative, not a host binding: the element's id may already be owned by another
+      // directive (e.g. Listbox, Tree, Grid), so this can't collide with it.
+      if (!el.id) {
+        el.id = this._idGenerator.getId('ng-combobox-widget-', true);
+      }
+      // Set synchronously; the MutationObserver above only fires on the next microtask.
+      this.popupId.set(el.id);
+    });
   }
 
   ngOnInit() {
diff --git a/src/aria/combobox/combobox.spec.ts b/src/aria/combobox/combobox.spec.ts
index a3ee5b66d957..5f835a5d2a7f 100644
--- a/src/aria/combobox/combobox.spec.ts
+++ b/src/aria/combobox/combobox.spec.ts
@@ -3,6 +3,7 @@ import {
   computed,
   DebugElement,
   signal,
+  Type,
   untracked,
   viewChild,
   afterRenderEffect,
@@ -1235,6 +1236,47 @@ describe('Combobox', () => {
       });
     });
   });
+
+  describe('ComboboxWidget', () => {
+    let fixture: ComponentFixture<unknown>;
+    let comboboxElement: HTMLElement;
+    let widgetElement: HTMLElement;
+
+    const expand = async (componentType: Type<unknown>) => {
+      fixture = TestBed.createComponent(componentType);
+      await fixture.whenStable();
+      comboboxElement = fixture.debugElement.query(By.directive(Combobox))
+        .nativeElement as HTMLElement;
+      comboboxElement.dispatchEvent(new FocusEvent('focusin', {bubbles: true}));
+      await fixture.whenStable();
+      comboboxElement.dispatchEvent(
+        new KeyboardEvent('keydown', {key: 'ArrowDown', bubbles: true}),
+      );
+      await fixture.whenStable();
+      widgetElement = fixture.debugElement.query(By.directive(ComboboxWidget))
+        .nativeElement as HTMLElement;
+    };
+
+    afterEach(async () => await runAccessibilityChecks(fixture.nativeElement));
+
+    it('should auto-generate an ID on the widget when none is provided', async () => {
+      await expand(ComboboxDialogExample);
+      expect(widgetElement.id).toMatch(/^ng-combobox-widget-/);
+      expect(comboboxElement.getAttribute('aria-controls')).toBe(widgetElement.id);
+    });
+
+    it('should preserve an explicit ID on the widget element', async () => {
+      await expand(ComboboxDialogCustomIdExample);
+      expect(widgetElement.id).toBe('custom-id');
+      expect(comboboxElement.getAttribute('aria-controls')).toBe('custom-id');
+    });
+
+    it('should prioritize sibling directive IDs over generated IDs', async () => {
+      await expand(ComboboxListboxGeneratedIdExample);
+      expect(widgetElement.id).toMatch(/^ng-listbox-/);
+      expect(comboboxElement.getAttribute('aria-controls')).toBe(widgetElement.id);
+    });
+  });
 });
 
 @Component({
@@ -1716,3 +1758,77 @@ class ComboboxListboxHighlightExample {
     this.popupExpanded.set(false);
   }
 }
+
+@Component({
+  template: `
+<div>
+  <div
+    ngCombobox
+    #combobox="ngCombobox"
+    aria-label="Search"
+    [(expanded)]="popupExpanded"
+  >{{value()}}</div>
+
+  <ng-template ngComboboxPopup [combobox]="combobox" popupType="dialog">
+    <div ngComboboxWidget>
+      <input aria-label="Filter" />
+    </div>
+  </ng-template>
+</div>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget],
+})
+class ComboboxDialogExample {
+  popupExpanded = signal(false);
+  value = signal('');
+}
+
+@Component({
+  template: `
+<div>
+  <div
+    ngCombobox
+    #combobox="ngCombobox"
+    aria-label="Search"
+    [(expanded)]="popupExpanded"
+  >{{value()}}</div>
+
+  <ng-template ngComboboxPopup [combobox]="combobox" popupType="dialog">
+    <div ngComboboxWidget id="custom-id">
+      <input aria-label="Filter" />
+    </div>
+  </ng-template>
+</div>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget],
+})
+class ComboboxDialogCustomIdExample {
+  popupExpanded = signal(false);
+  value = signal('');
+}
+
+@Component({
+  template: `
+<div>
+  <input
+    ngCombobox
+    #combobox="ngCombobox"
+    aria-label="Search"
+    [(expanded)]="popupExpanded"
+  />
+
+  <ng-template ngComboboxPopup [combobox]="combobox">
+    <div ngComboboxWidget ngListbox #listbox="ngListbox" focusMode="activedescendant" [activeDescendant]="listbox.activeDescendant()">
+      @for (option of options; track option) {
+        <div ngOption [value]="option" [label]="option">{{option}}</div>
+      }
+    </div>
+  </ng-template>
+</div>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget, Listbox, Option],
+})
+class ComboboxListboxGeneratedIdExample {
+  popupExpanded = signal(false);
+  options = ['Apple', 'Banana'];
+}