diff --git a/src/cdk/drag-drop/directives/drag-handle.ts b/src/cdk/drag-drop/directives/drag-handle.ts
index 9dd1bd514181..01d11aa430c8 100644
--- a/src/cdk/drag-drop/directives/drag-handle.ts
+++ b/src/cdk/drag-drop/directives/drag-handle.ts
@@ -7,6 +7,7 @@
  */
 
 import {
+  AfterViewInit,
   Directive,
   ElementRef,
   InjectionToken,
@@ -19,6 +20,7 @@ import {Subject} from 'rxjs';
 import type {CdkDrag} from './drag';
 import {CDK_DRAG_PARENT} from '../drag-parent';
 import {assertElementNode} from './assertions';
+import {DragDropRegistry} from '../drag-drop-registry';
 
 /**
  * Injection token that can be used to reference instances of `CdkDragHandle`. It serves as
@@ -35,10 +37,11 @@ export const CDK_DRAG_HANDLE = new InjectionToken<CdkDragHandle>('CdkDragHandle'
   },
   providers: [{provide: CDK_DRAG_HANDLE, useExisting: CdkDragHandle}],
 })
-export class CdkDragHandle implements OnDestroy {
+export class CdkDragHandle implements AfterViewInit, OnDestroy {
   element = inject<ElementRef<HTMLElement>>(ElementRef);
 
   private _parentDrag = inject<CdkDrag>(CDK_DRAG_PARENT, {optional: true, skipSelf: true});
+  private _dragDropRegistry = inject(DragDropRegistry);
 
   /** Emits when the state of the handle has changed. */
   readonly _stateChanges = new Subject<CdkDragHandle>();
@@ -64,6 +67,21 @@ export class CdkDragHandle implements OnDestroy {
     this._parentDrag?._addHandle(this);
   }
 
+  ngAfterViewInit() {
+    if (!this._parentDrag) {
+      let parent = this.element.nativeElement.parentElement;
+      while (parent) {
+        const ref = this._dragDropRegistry.getDragDirectiveForNode(parent);
+        if (ref) {
+          this._parentDrag = ref;
+          ref._addHandle(this);
+          break;
+        }
+        parent = parent.parentElement;
+      }
+    }
+  }
+
   ngOnDestroy() {
     this._parentDrag?._removeHandle(this);
     this._stateChanges.complete();
diff --git a/src/cdk/drag-drop/directives/drag.ts b/src/cdk/drag-drop/directives/drag.ts
index 11535b2bdf2a..8ec7fab27f5e 100644
--- a/src/cdk/drag-drop/directives/drag.ts
+++ b/src/cdk/drag-drop/directives/drag.ts
@@ -48,8 +48,7 @@ import type {CdkDropList} from './drop-list';
 import {DragDrop} from '../drag-drop';
 import {CDK_DRAG_CONFIG, DragDropConfig, DragStartDelay, DragAxis} from './config';
 import {assertElementNode} from './assertions';
-
-const DRAG_HOST_CLASS = 'cdk-drag';
+import {DragDropRegistry} from '../drag-drop-registry';
 
 /**
  * Injection token that can be used to reference instances of `CdkDropList`. It serves as
@@ -63,7 +62,7 @@ export const CDK_DROP_LIST = new InjectionToken<CdkDropList>('CdkDropList');
   selector: '[cdkDrag]',
   exportAs: 'cdkDrag',
   host: {
-    'class': DRAG_HOST_CLASS,
+    'class': 'cdk-drag',
     '[class.cdk-drag-disabled]': 'disabled',
     '[class.cdk-drag-dragging]': '_dragRef.isDragging()',
   },
@@ -78,9 +77,9 @@ export class CdkDrag<T = any> implements AfterViewInit, OnChanges, OnDestroy {
   private _changeDetectorRef = inject(ChangeDetectorRef);
   private _selfHandle = inject<CdkDragHandle>(CDK_DRAG_HANDLE, {optional: true, self: true});
   private _parentDrag = inject<CdkDrag>(CDK_DRAG_PARENT, {optional: true, skipSelf: true});
+  private _dragDropRegistry = inject(DragDropRegistry);
 
   private readonly _destroyed = new Subject<void>();
-  private static _dragInstances: CdkDrag[] = [];
   private _handles = new BehaviorSubject<CdkDragHandle[]>([]);
   private _previewTemplate: CdkDragPreview | null;
   private _placeholderTemplate: CdkDragPlaceholder | null;
@@ -240,11 +239,7 @@ export class CdkDrag<T = any> implements AfterViewInit, OnChanges, OnDestroy {
       zIndex: config?.zIndex,
     });
     this._dragRef.data = this;
-
-    // We have to keep track of the drag instances in order to be able to match an element to
-    // a drag instance. We can't go through the global registry of `DragRef`, because the root
-    // element could be different.
-    CdkDrag._dragInstances.push(this);
+    this._dragDropRegistry.registerDirectiveNode(this.element.nativeElement, this);
 
     if (config) {
       this._assignDefaults(config);
@@ -348,10 +343,7 @@ export class CdkDrag<T = any> implements AfterViewInit, OnChanges, OnDestroy {
       this.dropContainer.removeItem(this);
     }
 
-    const index = CdkDrag._dragInstances.indexOf(this);
-    if (index > -1) {
-      CdkDrag._dragInstances.splice(index, 1);
-    }
+    this._dragDropRegistry.removeDirectiveNode(this.element.nativeElement);
 
     // Unnecessary in most cases, but used to avoid extra change detections with `zone-paths-rxjs`.
     this._ngZone.runOutsideAngular(() => {
@@ -487,12 +479,9 @@ export class CdkDrag<T = any> implements AfterViewInit, OnChanges, OnDestroy {
       // the item was projected into another item by something like `ngTemplateOutlet`.
       let parent = this.element.nativeElement.parentElement;
       while (parent) {
-        if (parent.classList.contains(DRAG_HOST_CLASS)) {
-          ref.withParent(
-            CdkDrag._dragInstances.find(drag => {
-              return drag.element.nativeElement === parent;
-            })?._dragRef || null,
-          );
+        const parentDrag = this._dragDropRegistry.getDragDirectiveForNode(parent);
+        if (parentDrag) {
+          ref.withParent(parentDrag._dragRef);
           break;
         }
         parent = parent.parentElement;
diff --git a/src/cdk/drag-drop/directives/standalone-drag.spec.ts b/src/cdk/drag-drop/directives/standalone-drag.spec.ts
index 775f9e69ef91..c4449abe204e 100644
--- a/src/cdk/drag-drop/directives/standalone-drag.spec.ts
+++ b/src/cdk/drag-drop/directives/standalone-drag.spec.ts
@@ -9,6 +9,7 @@ import {
   ViewEncapsulation,
   signal,
 } from '@angular/core';
+import {NgTemplateOutlet} from '@angular/common';
 import {fakeAsync, flush, tick} from '@angular/core/testing';
 import {
   dispatchEvent,
@@ -1631,6 +1632,25 @@ describe('Standalone CdkDrag', () => {
         .toBe('translate3d(50px, 100px, 0px)');
     }));
 
+    it('should be able to drag with a handle that is defined in a separate embedded view', fakeAsync(() => {
+      const fixture = createComponent(StandaloneDraggableWithExternalTemplateHandle);
+      fixture.detectChanges();
+      const dragElement = fixture.componentInstance.dragElement.nativeElement;
+      const handle = fixture.nativeElement.querySelector('.handle');
+
+      expect(dragElement.style.transform).toBeFalsy();
+      dragElementViaMouse(fixture, dragElement, 50, 100);
+
+      expect(dragElement.style.transform)
+        .withContext('Expected not to be able to drag the element by itself.')
+        .toBeFalsy();
+
+      dragElementViaMouse(fixture, handle, 50, 100);
+      expect(dragElement.style.transform)
+        .withContext('Expected to drag the element by its handle.')
+        .toBe('translate3d(50px, 100px, 0px)');
+    }));
+
     it('should disable the tap highlight while dragging via the handle', fakeAsync(() => {
       // This test is irrelevant if the browser doesn't support styling the tap highlight color.
       if (!('webkitTapHighlightColor' in document.body.style)) {
@@ -2010,3 +2030,21 @@ class DraggableNgContainerWithAlternateRoot {
 class PlainStandaloneDraggable {
   @ViewChild(CdkDrag) dragInstance: CdkDrag;
 }
+
+@Component({
+  template: `
+    <div #dragElement cdkDrag
+      style="width: 100px; height: 100px; background: red; position: relative">
+      <ng-container [ngTemplateOutlet]="template"/>
+    </div>
+
+    <ng-template #template>
+      <div cdkDragHandle class="handle" style="width: 10px; height: 10px; background: green;"></div>
+    </ng-template>
+  `,
+  standalone: true,
+  imports: [CdkDrag, CdkDragHandle, NgTemplateOutlet],
+})
+class StandaloneDraggableWithExternalTemplateHandle {
+  @ViewChild('dragElement') dragElement: ElementRef<HTMLElement>;
+}
diff --git a/src/cdk/drag-drop/drag-drop-registry.ts b/src/cdk/drag-drop/drag-drop-registry.ts
index 3c789a2f933b..a8e2bd079fc7 100644
--- a/src/cdk/drag-drop/drag-drop-registry.ts
+++ b/src/cdk/drag-drop/drag-drop-registry.ts
@@ -23,6 +23,7 @@ import {_CdkPrivateStyleLoader} from '@angular/cdk/private';
 import {Observable, Observer, Subject, merge} from 'rxjs';
 import type {DropListRef} from './drop-list-ref';
 import type {DragRef} from './drag-ref';
+import type {CdkDrag} from './directives/drag';
 
 /** Event options that can be used to bind an active, capturing event. */
 const activeCapturingEventOptions = normalizePassiveListenerOptions({
@@ -79,6 +80,13 @@ export class DragDropRegistry<_ = unknown, __ = unknown> implements OnDestroy {
    */
   private _draggingPredicate = (item: DragRef) => item.isDragging();
 
+  /**
+   * Map tracking DOM nodes and their corresponding drag directives. Note that this is different
+   * from looking through the `_dragInstances` and getting their root node, because the root node
+   * isn't necessarily the node that the directive is set on.
+   */
+  private _domNodesToDirectives: WeakMap<Node, CdkDrag> | null = null;
+
   /**
    * Emits the `touchmove` or `mousemove` events that are dispatched
    * while the user is dragging a drag item instance.
@@ -262,9 +270,36 @@ export class DragDropRegistry<_ = unknown, __ = unknown> implements OnDestroy {
     return merge(...streams);
   }
 
+  /**
+   * Tracks the DOM node which has a draggable directive.
+   * @param node Node to track.
+   * @param dragRef Drag directive set on the node.
+   */
+  registerDirectiveNode(node: Node, dragRef: CdkDrag): void {
+    this._domNodesToDirectives ??= new WeakMap();
+    this._domNodesToDirectives.set(node, dragRef);
+  }
+
+  /**
+   * Stops tracking a draggable directive node.
+   * @param node Node to stop tracking.
+   */
+  removeDirectiveNode(node: Node): void {
+    this._domNodesToDirectives?.delete(node);
+  }
+
+  /**
+   * Gets the drag directive corresponding to a specific DOM node, if any.
+   * @param node Node for which to do the lookup.
+   */
+  getDragDirectiveForNode(node: Node): CdkDrag | null {
+    return this._domNodesToDirectives?.get(node) || null;
+  }
+
   ngOnDestroy() {
     this._dragInstances.forEach(instance => this.removeDragItem(instance));
     this._dropInstances.forEach(instance => this.removeDropContainer(instance));
+    this._domNodesToDirectives = null;
     this._clearGlobalListeners();
     this.pointerMove.complete();
     this.pointerUp.complete();
diff --git a/tools/public_api_guard/cdk/drag-drop.md b/tools/public_api_guard/cdk/drag-drop.md
index bb39566f6fdc..0624dfeb708b 100644
--- a/tools/public_api_guard/cdk/drag-drop.md
+++ b/tools/public_api_guard/cdk/drag-drop.md
@@ -150,7 +150,7 @@ export interface CdkDragExit<T = any, I = T> {
 }
 
 // @public
-export class CdkDragHandle implements OnDestroy {
+export class CdkDragHandle implements AfterViewInit, OnDestroy {
     constructor(...args: unknown[]);
     get disabled(): boolean;
     set disabled(value: boolean);
@@ -159,6 +159,8 @@ export class CdkDragHandle implements OnDestroy {
     // (undocumented)
     static ngAcceptInputType_disabled: unknown;
     // (undocumented)
+    ngAfterViewInit(): void;
+    // (undocumented)
     ngOnDestroy(): void;
     readonly _stateChanges: Subject<CdkDragHandle>;
     // (undocumented)
@@ -351,13 +353,16 @@ export class DragDropModule {
 // @public
 export class DragDropRegistry<_ = unknown, __ = unknown> implements OnDestroy {
     constructor(...args: unknown[]);
+    getDragDirectiveForNode(node: Node): CdkDrag | null;
     isDragging(drag: DragRef): boolean;
     // (undocumented)
     ngOnDestroy(): void;
     readonly pointerMove: Subject<TouchEvent | MouseEvent>;
     readonly pointerUp: Subject<TouchEvent | MouseEvent>;
+    registerDirectiveNode(node: Node, dragRef: CdkDrag): void;
     registerDragItem(drag: DragRef): void;
     registerDropContainer(drop: DropListRef): void;
+    removeDirectiveNode(node: Node): void;
     removeDragItem(drag: DragRef): void;
     removeDropContainer(drop: DropListRef): void;
     // @deprecated