diff --git a/packages/core/src/Combobox/Combobox.test.ts b/packages/core/src/Combobox/Combobox.test.ts
index a02fc7b94..874ba4be6 100644
--- a/packages/core/src/Combobox/Combobox.test.ts
+++ b/packages/core/src/Combobox/Combobox.test.ts
@@ -2,8 +2,9 @@ import type { DOMWrapper, VueWrapper } from '@vue/test-utils'
 import { mount } from '@vue/test-utils'
 import { beforeEach, describe, expect, it, vi } from 'vitest'
 import { axe } from 'vitest-axe'
-import { nextTick } from 'vue'
+import { defineComponent, h, nextTick, ref } from 'vue'
 import { handleSubmit, sleep } from '@/test'
+import { ComboboxAnchor, ComboboxContent, ComboboxInput, ComboboxItem, ComboboxRoot, ComboboxTrigger, ComboboxViewport } from '.'
 import Combobox from './story/_Combobox.vue'
 import ComboboxObject from './story/_ComboboxObject.vue'
 import ComboboxTagsInput from './story/_ComboboxTagsInput.vue'
@@ -542,3 +543,93 @@ describe('given combobox handleBlur with deferred close', () => {
     externalButton.remove()
   })
 })
+
+describe('comboboxContent with popper positioning', () => {
+  const getSlotRenderCount = vi.fn(() => ({ value: 0 }))
+
+  const PopperCombobox = defineComponent({
+    setup() {
+      const modelValue = ref('')
+      const slotRenderCount = getSlotRenderCount()
+      const options = Array.from({ length: 60 }, (_, index) => `Option ${index}`)
+
+      return () => h(ComboboxRoot, {
+        'modelValue': modelValue.value,
+        'onUpdate:modelValue': (value: string) => modelValue.value = value,
+      }, {
+        default: () => [
+          h(ComboboxAnchor, null, {
+            default: () => [
+              h(ComboboxInput),
+              h(ComboboxTrigger, null, { default: () => 'Open' }),
+            ],
+          }),
+          h(ComboboxContent, { position: 'popper' }, {
+            default: () => {
+              slotRenderCount.value += 1
+              return h(ComboboxViewport, null, {
+                default: () => options.map(option => h(ComboboxItem, { key: option, value: option }, { default: () => option })),
+              })
+            },
+          }),
+        ],
+      })
+    },
+  })
+
+  beforeEach(() => {
+    document.body.innerHTML = ''
+    getSlotRenderCount.mockClear()
+    globalThis.ResizeObserver = class ResizeObserver {
+      private callback: ResizeObserverCallback
+
+      constructor(callback: ResizeObserverCallback) {
+        this.callback = callback
+      }
+
+      observe(target: Element) {
+        this.callback([{ target } as ResizeObserverEntry], this)
+        this.callback([{ target } as ResizeObserverEntry], this)
+      }
+
+      unobserve() {}
+      disconnect() {}
+    }
+  })
+
+  it('does not rerender option slot content after popper position updates', async () => {
+    const slotRenderCount = { value: 0 }
+    getSlotRenderCount.mockReturnValue(slotRenderCount)
+
+    const wrapper = mount(PopperCombobox, { attachTo: document.body })
+
+    await wrapper.find('button').trigger('click')
+    await nextTick()
+
+    expect(slotRenderCount.value).toBe(3)
+
+    await sleep(0)
+    await nextTick()
+
+    expect(slotRenderCount.value).toBe(4)
+  })
+
+  it('updates visible options when filtering while popper content is open', async () => {
+    const slotRenderCount = { value: 0 }
+    getSlotRenderCount.mockReturnValue(slotRenderCount)
+
+    const wrapper = mount(PopperCombobox, { attachTo: document.body })
+
+    await wrapper.find('button').trigger('click')
+    await nextTick()
+
+    expect(wrapper.text()).toContain('Option 1')
+    expect(wrapper.text()).toContain('Option 59')
+
+    await wrapper.find('input').setValue('Option 59')
+    await nextTick()
+
+    expect(wrapper.text()).toContain('Option 59')
+    expect(wrapper.text()).not.toContain('Option 1')
+  })
+})
diff --git a/packages/core/src/Combobox/ComboboxContentImpl.vue b/packages/core/src/Combobox/ComboboxContentImpl.vue
index ab6f1ee47..966ad12d7 100644
--- a/packages/core/src/Combobox/ComboboxContentImpl.vue
+++ b/packages/core/src/Combobox/ComboboxContentImpl.vue
@@ -128,6 +128,9 @@ onUnmounted(() => {
           v-bind="{ ...$attrs, ...forwardedProps }"
           :id="rootContext.contentId"
           :ref="forwardRef"
+          :memo-dependencies="position === 'popper'
+            ? [rootContext.filterSearch.value, rootContext.filterState.value]
+            : undefined"
           :data-state="rootContext.open.value ? 'open' : 'closed'"
           :data-empty="isEmpty ? '' : undefined"
           :style="{
diff --git a/packages/core/src/Combobox/ComboboxItem.vue b/packages/core/src/Combobox/ComboboxItem.vue
index df40d116c..a39daf2bd 100644
--- a/packages/core/src/Combobox/ComboboxItem.vue
+++ b/packages/core/src/Combobox/ComboboxItem.vue
@@ -80,6 +80,7 @@ onUnmounted(() => {
     v-bind="props"
     :id="id"
     ref="primitiveElement"
+    v-memo="[isRender, rootContext.filterSearch.value, rootContext.disabled.value, disabled, props.value, props.as, props.asChild, ...Object.values($attrs)]"
     :disabled="rootContext.disabled.value || disabled"
     @select="(event) => {
       emits('select', event as any)
diff --git a/packages/core/src/Popper/PopperContent.vue b/packages/core/src/Popper/PopperContent.vue
index b7e7b1623..0a6cc2b03 100644
--- a/packages/core/src/Popper/PopperContent.vue
+++ b/packages/core/src/Popper/PopperContent.vue
@@ -32,6 +32,11 @@ export const PopperContentPropsDefaultValue = {
 }
 
 export interface PopperContentProps extends PrimitiveProps {
+  /**
+   * Reactive dependencies that should invalidate the memoized content subtree.
+   */
+  memoDependencies?: unknown[]
+
   /**
    * The preferred side of the trigger to render against when open.
    * Will be reversed when collisions occur and avoidCollisions
@@ -402,10 +407,37 @@ providePopperContentContext({
     }"
   >
     <Primitive
+      v-if="props.memoDependencies"
+      :ref="forwardRef"
+      v-memo="[
+        props.asChild,
+        props.as,
+        placedSide,
+        placedAlign,
+        isPositioned,
+        ...Object.values($attrs),
+        ...props.memoDependencies,
+      ]"
+      v-bind="$attrs"
+      :as-child="props.asChild"
+      :as="props.as"
+      :data-side="placedSide"
+      :data-align="placedAlign"
+      :style="{
+        // if the PopperContent hasn't been placed yet (not all measurements done)
+        // we prevent animations so that users's animation don't kick in too early referring wrong sides
+        animation: !isPositioned ? 'none' : undefined,
+      }"
+    >
+      <slot />
+    </Primitive>
+
+    <Primitive
+      v-else
       :ref="forwardRef"
       v-bind="$attrs"
       :as-child="props.asChild"
-      :as="as"
+      :as="props.as"
       :data-side="placedSide"
       :data-align="placedAlign"
       :style="{