diff --git a/packages/runtime-core/src/index.ts b/packages/runtime-core/src/index.ts
index 94b2985040a..b281da1e717 100644
--- a/packages/runtime-core/src/index.ts
+++ b/packages/runtime-core/src/index.ts
@@ -354,6 +354,8 @@ export {
   normalizeStyle,
 } from '@vue/shared'
 
+export { filterSingleRoot } from './componentRenderUtils'
+
 // For test-utils
 export { transformVNodeArgs } from './vnode'
 
diff --git a/packages/runtime-dom/src/components/TransitionGroup.ts b/packages/runtime-dom/src/components/TransitionGroup.ts
index f98e82b2734..97a5592ce8e 100644
--- a/packages/runtime-dom/src/components/TransitionGroup.ts
+++ b/packages/runtime-dom/src/components/TransitionGroup.ts
@@ -15,8 +15,10 @@ import {
   Fragment,
   type SetupContext,
   type VNode,
+  type VNodeArrayChildren,
   compatUtils,
   createVNode,
+  filterSingleRoot,
   getCurrentInstance,
   getTransitionRawChildren,
   onUpdated,
@@ -26,7 +28,7 @@ import {
   useTransitionState,
   warn,
 } from '@vue/runtime-core'
-import { extend } from '@vue/shared'
+import { PatchFlags, ShapeFlags, extend } from '@vue/shared'
 
 const positionMap = new WeakMap<VNode, DOMRect>()
 const newPositionMap = new WeakMap<VNode, DOMRect>()
@@ -113,6 +115,28 @@ const TransitionGroupImpl: ComponentOptions = {
       }
 
       prevChildren = children
+
+      // In dev mode, comments are preserved, and it's possible for a template
+      // to have comments alongside the root element which makes it a fragment.
+      // In that case we re-assign `el` so DOM operations access the actual
+      // root element instead of the fragment root. (#6745)
+      if (__DEV__ && prevChildren) {
+        prevChildren.forEach(child => {
+          if (
+            child.shapeFlag & ShapeFlags.COMPONENT &&
+            child.component &&
+            child.component.subTree.patchFlag & PatchFlags.DEV_ROOT_FRAGMENT
+          ) {
+            const elementRoot = filterSingleRoot(
+              child.component.subTree.children as VNodeArrayChildren,
+            )
+            if (elementRoot) {
+              child.el = elementRoot.el
+            }
+          }
+        })
+      }
+
       children = slots.default ? getTransitionRawChildren(slots.default()) : []
 
       for (let i = 0; i < children.length; i++) {
diff --git a/packages/vue/__tests__/e2e/TransitionGroup.spec.ts b/packages/vue/__tests__/e2e/TransitionGroup.spec.ts
index febc9d3c20a..4f52d4a8e06 100644
--- a/packages/vue/__tests__/e2e/TransitionGroup.spec.ts
+++ b/packages/vue/__tests__/e2e/TransitionGroup.spec.ts
@@ -508,4 +508,45 @@ describe('e2e: TransitionGroup', () => {
 
     expect(`<TransitionGroup> children must be keyed`).toHaveBeenWarned()
   })
+
+  test(
+    'works when child component has single root + comments',
+    async () => {
+      const onErrorSpy = vi.fn()
+      await page().exposeFunction('onErrorSpy', onErrorSpy)
+
+      await page().evaluate(() => {
+        const { onErrorSpy } = window as any
+        const { createApp, ref, onErrorCaptured } = (window as any).Vue
+
+        const app = createApp({
+          template: `
+          <div id="container">
+            <transition-group>
+              <a-component v-if="show"></a-component>
+            </transition-group>
+          </div>
+          <button id="toggleBtn" @click="click">button</button>
+          `,
+          setup: () => {
+            onErrorCaptured(() => onErrorSpy())
+            const show = ref(true)
+            const click = () => (show.value = false)
+            return { show, click }
+          },
+        })
+        app.component('a-component', { template: `<!----><div></div>` })
+        app.mount('#app')
+      })
+
+      expect(await html('#container')).toBe('<!----><div></div>')
+
+      await htmlWhenTransitionStart()
+      await transitionFinish()
+
+      expect(onErrorSpy).not.toBeCalled()
+      expect(await html('#container')).toBe('')
+    },
+    E2E_TIMEOUT,
+  )
 })