--- a/toolkit/components/extensions/ExtensionChild.jsm
+++ b/toolkit/components/extensions/ExtensionChild.jsm
@@ -1029,16 +1029,19 @@ class ChildAPIManager {
       addListener: (listener, ...args) => impl.addListener(listener, args),
       removeListener: (listener) => impl.removeListener(listener),
       hasListener: (listener) => impl.hasListener(listener),
     };
   }
 
   close() {
     this.messageManager.sendAsyncMessage("API:CloseProxyContext", {childId: this.id});
+    this.messageManager.removeMessageListener("API:CallResult", this);
+    MessageChannel.removeListener(this.messageManager, "API:RunListener", this);
+
     if (this.updatePermissions) {
       this.context.extension.off("add-permissions", this.updatePermissions);
       this.context.extension.off("remove-permissions", this.updatePermissions);
     }
   }
 
   get cloneScope() {
     return this.context.cloneScope;

new file mode 100644
--- /dev/null
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_contexts_gc.js
@@ -0,0 +1,128 @@
+"use strict";
+
+const server = createHttpServer();
+server.registerDirectory("/data/", do_get_file("data"));
+
+const BASE_URL = `http://localhost:${server.identity.primaryPort}/data`;
+
+// ExtensionContent.jsm needs to know when it's running from xpcshell,
+// to use the right timeout for content scripts executed at document_idle.
+ExtensionTestUtils.mockAppInfo();
+
+// Each of these tests do the following:
+// 1. Load document to create an extension context (instance of BaseContext).
+// 2. Get weak reference to that context.
+// 3. Unload the document.
+// 4. Force GC and check that the weak reference has been invalidated.
+
+async function reloadTopContext(contentPage) {
+  await contentPage.spawn(null, async () => {
+    let {TestUtils} = ChromeUtils.import("resource://testing-common/TestUtils.jsm", {});
+    let windowNukeObserved = TestUtils.topicObserved("inner-window-nuked");
+    info(`Reloading top-level document`);
+    this.content.location.reload();
+    await windowNukeObserved;
+    info(`Reloaded top-level document`);
+  });
+}
+
+async function assertContextReleased(contentPage, description) {
+  await contentPage.spawn(description, async assertionDescription => {
+    // Force GC, see https://searchfox.org/mozilla-central/rev/b0275bc977ad7fda615ef34b822bba938f2b16fd/testing/talos/talos/tests/devtools/addon/content/damp.js#84-98
+    let gcCount = 0;
+    while (gcCount < 30 && this.contextWeakRef.get() !== null) {
+      ++gcCount;
+      Cu.forceGC();
+      Cu.forceCC();
+      Cu.forceGC();
+      await new Promise(resolve => this.content.setTimeout(resolve, 0));
+    }
+
+    // The above loop needs to be repeated at most 3 times according to MinimizeMemoryUsage:
+    // https://searchfox.org/mozilla-central/rev/6f86cc3479f80ace97f62634e2c82a483d1ede40/xpcom/base/nsMemoryReporterManager.cpp#2644-2647
+    Assert.lessOrEqual(gcCount, 3, `Context should have been GCd within a few GC attempts.`);
+
+    // Each test will set this.contextWeakRef before unloading the document.
+    Assert.ok(!this.contextWeakRef.get(), assertionDescription);
+  });
+}
+
+add_task(async function test_ContentScriptContextChild_in_child_frame() {
+  let extensionData = {
+    manifest: {
+      content_scripts: [
+        {
+          matches: ["http://*/*/file_iframe.html"],
+          js: ["content_script.js"],
+          all_frames: true,
+        },
+      ],
+    },
+
+    files: {
+      "content_script.js": "browser.test.sendMessage('contentScriptLoaded');",
+    },
+  };
+
+  let extension = ExtensionTestUtils.loadExtension(extensionData);
+  await extension.startup();
+
+  let contentPage = await ExtensionTestUtils.loadContentPage(`${BASE_URL}/file_toplevel.html`);
+  await extension.awaitMessage("contentScriptLoaded");
+
+  await contentPage.spawn(extension.id, async extensionId => {
+    let {DocumentManager} = ChromeUtils.import("resource://gre/modules/ExtensionContent.jsm", {});
+    let frame = this.content.document.querySelector("iframe[src*='file_iframe.html']");
+    let context = DocumentManager.getContext(extensionId, frame.contentWindow);
+
+    Assert.ok(context, "Got content script context");
+
+    this.contextWeakRef = Cu.getWeakReference(context);
+    frame.remove();
+  });
+
+  await assertContextReleased(contentPage, "ContentScriptContextChild should have been released");
+
+  await contentPage.close();
+  await extension.unload();
+});
+
+add_task(async function test_ContentScriptContextChild_in_toplevel() {
+  let extensionData = {
+    manifest: {
+      content_scripts: [
+        {
+          matches: ["http://*/*/file_sample.html"],
+          js: ["content_script.js"],
+          all_frames: true,
+        },
+      ],
+    },
+
+    files: {
+      "content_script.js": "browser.test.sendMessage('contentScriptLoaded');",
+    },
+  };
+
+  let extension = ExtensionTestUtils.loadExtension(extensionData);
+  await extension.startup();
+
+  let contentPage = await ExtensionTestUtils.loadContentPage(`${BASE_URL}/file_sample.html`);
+  await extension.awaitMessage("contentScriptLoaded");
+
+  await contentPage.spawn(extension.id, async extensionId => {
+    let {DocumentManager} = ChromeUtils.import("resource://gre/modules/ExtensionContent.jsm", {});
+    let context = DocumentManager.getContext(extensionId, this.content);
+
+    Assert.ok(context, "Got content script context");
+
+    this.contextWeakRef = Cu.getWeakReference(context);
+  });
+
+  await reloadTopContext(contentPage);
+  await extension.awaitMessage("contentScriptLoaded");
+  await assertContextReleased(contentPage, "ContentScriptContextChild should have been released");
+
+  await contentPage.close();
+  await extension.unload();
+});

--- a/toolkit/components/extensions/test/xpcshell/xpcshell-content.ini
+++ b/toolkit/components/extensions/test/xpcshell/xpcshell-content.ini
@@ -3,11 +3,12 @@ skip-if = os == "android" || (os == "win
 [test_ext_i18n_css.js]
 [test_ext_contentscript.js]
 [test_ext_contentscript_scriptCreated.js]
 skip-if = debug # Bug 1407501
 [test_ext_contentscript_triggeringPrincipal.js]
 skip-if = (os == "android" && debug) || (os == "win" && debug) # Windows: Bug 1438796
 [test_ext_contentscript_xrays.js]
 [test_ext_contentScripts_register.js]
+[test_ext_contexts_gc.js]
 skip-if = os == "android"
 [test_ext_adoption_with_xrays.js]
 [test_ext_shadowdom.js]