diff --git a/.gitignore b/.gitignore
index 156c78353e8..8c6d07e3109 100644
--- a/.gitignore
+++ b/.gitignore
@@ -28,6 +28,7 @@ test/tmp
 test/version_tmp
 test_*.html
 /tests/ember-tests.js
+/smoke-tests/scenarios/output/
 tmp
 tmp*.gem
 tmp.bpm
diff --git a/packages/@ember/-internals/glimmer/lib/renderer.ts b/packages/@ember/-internals/glimmer/lib/renderer.ts
index a1a177fd924..a1b65103013 100644
--- a/packages/@ember/-internals/glimmer/lib/renderer.ts
+++ b/packages/@ember/-internals/glimmer/lib/renderer.ts
@@ -227,6 +227,8 @@ class ClassicRootState {
 
       let result = (this.result = iterator.sync());
 
+      associateDestroyableChild(owner, result);
+
       // override .render function after initial render
       this.render = errorLoopTransaction(() => result.rerender({ alwaysRevalidate: false }));
     });
@@ -648,6 +650,10 @@ export function renderComponent(
 
   let innerResult = renderer.render(component, { into, args }).result;
 
+  if (innerResult) {
+    associateDestroyableChild(owner, innerResult);
+  }
+
   let result = {
     destroy() {
       if (innerResult) {
diff --git a/packages/@ember/-internals/glimmer/tests/integration/components/render-component-test.ts b/packages/@ember/-internals/glimmer/tests/integration/components/render-component-test.ts
index 1bac4bea6aa..abd3279d51f 100644
--- a/packages/@ember/-internals/glimmer/tests/integration/components/render-component-test.ts
+++ b/packages/@ember/-internals/glimmer/tests/integration/components/render-component-test.ts
@@ -18,7 +18,7 @@ import { array, concat, fn, get, hash, on } from '@glimmer/runtime';
 import GlimmerishComponent from '../../utils/glimmerish-component';
 
 import { run } from '@ember/runloop';
-import { associateDestroyableChild, registerDestructor } from '@glimmer/destroyable';
+import { destroy, associateDestroyableChild, registerDestructor } from '@glimmer/destroyable';
 import { renderComponent, type RenderResult } from '../../../lib/renderer';
 import { trackedObject } from '@ember/reactive/collections';
 import { cached, tracked } from '@glimmer/tracking';
@@ -80,17 +80,126 @@ class RenderComponentTestCase extends AbstractStrictTestCase {
   }
 }
 
+moduleFor(
+  'Strict Mode - RenderComponentTestCase',
+  class extends RenderComponentTestCase {
+    afterEach() {
+      if (this.component) {
+        runDestroy(this);
+      }
+    }
+
+    '@test destroy cleans up dom via destrying the test context'() {
+      let Foo = defComponent('Hello, world!');
+      let Root = defComponent('<Foo/>', { scope: { Foo } });
+
+      this.renderComponent(Root, { expect: 'Hello, world!' });
+
+      run(() => destroy(this));
+
+      assertHTML('');
+    }
+
+    '@test destroy of the owner cleans up dom via destrying the test context'() {
+      let Foo = defComponent('Hello, world!');
+      let Root = defComponent('<Foo/>', { scope: { Foo } });
+
+      this.renderComponent(Root, { expect: 'Hello, world!' });
+
+      run(() => destroy(this.owner));
+
+      assertHTML('');
+    }
+  }
+);
+
+moduleFor(
+  'Strict Mode - renderComponent (direct)',
+  class extends AbstractStrictTestCase {
+    get element() {
+      return document.querySelector('#qunit-fixture')!;
+    }
+
+    '@test manually calling destroy cleans up the DOM'() {
+      let Foo = defComponent('Hello, world!');
+
+      let owner = buildOwner({});
+      let manualDestroy: () => void;
+
+      run(() => {
+        let result = renderComponent(Foo, {
+          owner,
+          into: this.element,
+        });
+        manualDestroy = result.destroy;
+        this.component = {
+          ...result,
+          rerender() {
+            // unused, but asserted against
+          },
+        };
+      });
+
+      assertHTML('Hello, world!');
+      this.assertStableRerender();
+
+      run(() => manualDestroy());
+
+      assertHTML('');
+      this.assertStableRerender();
+
+      run(() => destroy(owner));
+    }
+
+    '@test destroying the owner cleans up the DOM'() {
+      let Foo = defComponent('Hello, world!');
+
+      let owner = buildOwner({});
+
+      run(() => {
+        let result = renderComponent(Foo, {
+          owner,
+          into: this.element,
+        });
+        this.component = {
+          ...result,
+          rerender() {
+            // unused, but asserted against
+          },
+        };
+      });
+
+      assertHTML('Hello, world!');
+      this.assertStableRerender();
+
+      run(() => destroy(owner));
+
+      assertHTML('');
+      this.assertStableRerender();
+    }
+  }
+);
+
 moduleFor(
   'Strict Mode - renderComponent',
   class extends RenderComponentTestCase {
     afterEach() {
       if (this.component) {
-        // runDestroy(this.component);
-        // runDestroy(this.owner);
         runDestroy(this);
       }
     }
 
+    '@test destroy cleans up dom via destroying the owner'() {
+      let Foo = defComponent('Hello, world!');
+      let Root = defComponent('<Foo/>', { scope: { Foo } });
+
+      this.renderComponent(Root, { expect: 'Hello, world!' });
+
+      run(() => destroy(this.owner));
+
+      assertHTML('');
+    }
+
     '@test Can use a component in scope'() {
       let Foo = defComponent('Hello, world!');
       let Root = defComponent('<Foo/>', { scope: { Foo } });
@@ -133,6 +242,24 @@ moduleFor(
       this.renderComponent(Root, { expect: 'foobar' });
     }
 
+    '@test multiple components have independent lifetimes'() {
+      class State {
+        @tracked showSecond = true;
+      }
+      let state = new State();
+      let Foo = defComponent('Hello, world!');
+      let Root = defComponent('<Foo />{{#if state.showSecond}}<Foo />{{/if}}', {
+        scope: { state, Foo },
+      });
+
+      this.renderComponent(Root, { expect: 'Hello, world!Hello, world!' });
+
+      this.assertChange({
+        change: () => (state.showSecond = false),
+        expect: 'Hello, world!<!---->',
+      });
+    }
+
     '@test Can use a dynamic component definition'() {
       let Foo = defComponent('Hello, world!');
       let Root = defComponent('<this.Foo/>', {
diff --git a/smoke-tests/scenarios/basic-test.ts b/smoke-tests/scenarios/basic-test.ts
index eecf94d563a..eee87411303 100644
--- a/smoke-tests/scenarios/basic-test.ts
+++ b/smoke-tests/scenarios/basic-test.ts
@@ -106,6 +106,84 @@ function basicTest(scenarios: Scenarios, appName: string) {
             `,
           },
           integration: {
+            'destruction-test.gjs': `
+              import { module, test } from 'qunit';
+              import { clearRender, render } from '@ember/test-helpers';
+              import { setupRenderingTest } from 'ember-qunit';
+              import { destroy, registerDestructor } from '@ember/destroyable';
+
+              import Component from '@glimmer/component';
+
+              class WillDestroy extends Component {
+                willDestroy() {
+                  super.willDestroy();
+                  this.args.onDestroy();
+                }
+              }
+
+              class Destructor extends Component {
+                constructor(...args) {
+                  super(...args);
+
+                  let onDestroy = this.args.onDestroy;
+                  registerDestructor(this, () => onDestroy());
+                }
+              }
+
+              module('@glimmer/component Destruction', function (hooks) {
+                setupRenderingTest(hooks);
+
+                module('after', function (hooks) {
+                  hooks.after(function (assert) {
+                    assert.verifySteps(['WillDestroy destroyed']);
+                  });
+
+                  test('it calls "@onDestroy"', async function (assert) {
+                    const onDestroy = () => assert.step('WillDestroy destroyed');
+
+                    await render(
+                      <template><WillDestroy @onDestroy={{onDestroy}} /></template>
+                    );
+                  });
+                });
+
+                module('afterEach', function (hooks) {
+                  hooks.afterEach(function (assert) {
+                    assert.verifySteps(['WillDestroy destroyed']);
+                  });
+
+                  test('it calls "@onDestroy"', async function (assert) {
+                    const onDestroy = () => assert.step('WillDestroy destroyed');
+
+                    await render(
+                      <template><WillDestroy @onDestroy={{onDestroy}} /></template>
+                    );
+
+                    destroy(this.owner);
+                  });
+                });
+
+                test('it calls "@onDestroy"', async function (assert) {
+                  const onDestroy = () => assert.step('destroyed');
+
+                  await render(<template><WillDestroy @onDestroy={{onDestroy}} /></template>);
+
+                  await clearRender();
+
+                  assert.verifySteps(['destroyed']);
+                });
+
+                test('it calls "registerDestructor"', async function (assert) {
+                  const onDestroy = () => assert.step('destroyed');
+
+                  await render(<template><Destructor @onDestroy={{onDestroy}} /></template>);
+
+                  await clearRender();
+
+                  assert.verifySteps(['destroyed']);
+                });
+              });
+            `,
             'interactive-example-test.js': `
               import { module, test } from 'qunit';
               import { setupRenderingTest } from 'ember-qunit';