diff --git a/dom/chrome-webidl/WebExtensionPolicy.webidl b/dom/chrome-webidl/WebExtensionPolicy.webidl
index cb88b3648a1a..806e6e991af1 100644
--- a/dom/chrome-webidl/WebExtensionPolicy.webidl
+++ b/dom/chrome-webidl/WebExtensionPolicy.webidl
@@ -94,6 +94,23 @@ interface WebExtensionPolicy {
    */
   static readonly attribute boolean isExtensionProcess;
 
+  /**
+   * Set based on the manifest.incognito value:
+   * If "spanning" or "split" will be true.
+   * If "not_allowed" will be false.
+   */
+  [Pure]
+  attribute boolean privateBrowsingAllowed;
+
+  /**
+   * Returns true if the extension can access a window.  Access is
+   * determined by matching the windows private browsing context
+   * with privateBrowsingMode.  This does not, and is not meant to
+   * handle specific differences between spanning and split mode.
+   */
+  [Affects=Nothing]
+  boolean canAccessWindow(WindowProxy window);
+
   /**
    * Returns true if the extension has cross-origin access to the given URI.
    */
@@ -193,4 +210,6 @@ dictionary WebExtensionInit {
   DOMString? contentSecurityPolicy = null;
 
   sequence<DOMString>? backgroundScripts = null;
+
+  boolean privateBrowsingAllowed = true;
 };
diff --git a/toolkit/components/extensions/Extension.jsm b/toolkit/components/extensions/Extension.jsm
index 18505b12e626..b77c11ec04e0 100644
--- a/toolkit/components/extensions/Extension.jsm
+++ b/toolkit/components/extensions/Extension.jsm
@@ -636,6 +636,7 @@ class ExtensionData {
       schemaURLs: null,
       type: this.type,
       webAccessibleResources,
+      privateBrowsingAllowed: manifest.incognito !== "not_allowed",
     };
 
     if (this.type === "extension") {
@@ -1599,6 +1600,14 @@ class Extension extends ExtensionData {
     return this.manifest.optional_permissions;
   }
 
+  get privateBrowsingAllowed() {
+    return this.policy.privateBrowsingAllowed;
+  }
+
+  canAccessWindow(window) {
+    return this.policy.canAccessWindow(window);
+  }
+
   // Representation of the extension to send to content
   // processes. This should include anything the content process might
   // need.
@@ -1615,6 +1624,7 @@ class Extension extends ExtensionData {
       whiteListedHosts: this.whiteListedHosts.patterns.map(pat => pat.pattern),
       permissions: this.permissions,
       optionalPermissions: this.optionalPermissions,
+      privateBrowsingAllowed: this.privateBrowsingAllowed,
     };
   }
 
@@ -1850,6 +1860,12 @@ class Extension extends ExtensionData {
         return;
       }
 
+      if (this.addonData && this.addonData.incognitoOverride !== undefined) {
+        this.policy.privateBrowsingAllowed = this.addonData.incognitoOverride !== "not_allowed";
+      } else {
+        this.policy.privateBrowsingAllowed = this.manifest.incognito !== "not_allowed";
+      }
+
       GlobalManager.init(this);
 
       this.initSharedData();
diff --git a/toolkit/components/extensions/ExtensionChild.jsm b/toolkit/components/extensions/ExtensionChild.jsm
index 3b628537393b..2e96faa710b7 100644
--- a/toolkit/components/extensions/ExtensionChild.jsm
+++ b/toolkit/components/extensions/ExtensionChild.jsm
@@ -712,6 +712,14 @@ class BrowserExtensionContent extends EventEmitter {
     return this._manifest;
   }
 
+  get privateBrowsingAllowed() {
+    return this.policy.privateBrowsingAllowed;
+  }
+
+  canAccessWindow(window) {
+    return this.policy.canAccessWindow(window);
+  }
+
   getAPIManager() {
     let apiManagers = [ExtensionPageChild.apiManager];
 
diff --git a/toolkit/components/extensions/ExtensionCommon.jsm b/toolkit/components/extensions/ExtensionCommon.jsm
index 745fb9a55a02..259ea7b1bf14 100644
--- a/toolkit/components/extensions/ExtensionCommon.jsm
+++ b/toolkit/components/extensions/ExtensionCommon.jsm
@@ -445,6 +445,14 @@ class BaseContext {
     return this.cloneScopePromise || this.cloneScope.Promise;
   }
 
+  get privateBrowsingAllowed() {
+    return this.extension.privateBrowsingAllowed;
+  }
+
+  canAccessWindow(window) {
+    return this.extension.canAccessWindow(window);
+  }
+
   setContentWindow(contentWindow) {
     this.innerWindowID = getInnerWindowID(contentWindow);
     this.messageManager = contentWindow.docShell.messageManager;
diff --git a/toolkit/components/extensions/ExtensionTestCommon.jsm b/toolkit/components/extensions/ExtensionTestCommon.jsm
index 24d0daada154..6bb53dfed329 100644
--- a/toolkit/components/extensions/ExtensionTestCommon.jsm
+++ b/toolkit/components/extensions/ExtensionTestCommon.jsm
@@ -368,6 +368,7 @@ var ExtensionTestCommon = class ExtensionTestCommon {
       resourceURI: jarURI,
       cleanupFile: file,
       signedState,
+      incognitoOverride: data.incognitoOverride,
       temporarilyInstalled: !!data.temporarilyInstalled,
       TEST_NO_ADDON_MANAGER: true,
     });
diff --git a/toolkit/components/extensions/WebExtensionContentScript.h b/toolkit/components/extensions/WebExtensionContentScript.h
index 7d856a164cf7..efbb8268147b 100644
--- a/toolkit/components/extensions/WebExtensionContentScript.h
+++ b/toolkit/components/extensions/WebExtensionContentScript.h
@@ -18,6 +18,7 @@
 #include "nsCOMPtr.h"
 #include "nsCycleCollectionParticipant.h"
 #include "nsISupports.h"
+#include "nsIDocShell.h"
 #include "nsWrapperCache.h"
 
 class nsILoadInfo;
@@ -67,6 +68,18 @@ class MOZ_STACK_CLASS DocInfo final {
     return nullptr;
   }
 
+  already_AddRefed<nsILoadContext> GetLoadContext() const {
+    nsCOMPtr<nsILoadContext> loadContext;
+    if (nsPIDOMWindowOuter* window = GetWindow()) {
+      nsIDocShell* docShell = window->GetDocShell();
+      loadContext = do_QueryInterface(docShell);
+    } else if (nsILoadInfo* loadInfo = GetLoadInfo()) {
+      nsCOMPtr<nsISupports> requestingContext = loadInfo->GetLoadingContext();
+      loadContext = do_QueryInterface(requestingContext);
+    }
+    return loadContext.forget();
+  }
+
  private:
   void SetURL(const URLInfo& aURL);
 
diff --git a/toolkit/components/extensions/WebExtensionPolicy.cpp b/toolkit/components/extensions/WebExtensionPolicy.cpp
index b401a24ed69f..9c66bd471a47 100644
--- a/toolkit/components/extensions/WebExtensionPolicy.cpp
+++ b/toolkit/components/extensions/WebExtensionPolicy.cpp
@@ -11,7 +11,6 @@
 #include "mozilla/AddonManagerWebAPI.h"
 #include "mozilla/ResultExtensions.h"
 #include "nsEscape.h"
-#include "nsIDocShell.h"
 #include "nsIObserver.h"
 #include "nsISubstitutingProtocolHandler.h"
 #include "nsNetUtil.h"
@@ -133,7 +132,8 @@ WebExtensionPolicy::WebExtensionPolicy(GlobalObject& aGlobal,
       mName(aInit.mName),
       mContentSecurityPolicy(aInit.mContentSecurityPolicy),
       mLocalizeCallback(aInit.mLocalizeCallback),
-      mPermissions(new AtomSet(aInit.mPermissions)) {
+      mPermissions(new AtomSet(aInit.mPermissions)),
+      mPrivateBrowsingAllowed(aInit.mPrivateBrowsingAllowed) {
   if (!ParseGlobs(aGlobal, aInit.mWebAccessibleResources, mWebAccessiblePaths,
                   aRv)) {
     return;
@@ -440,6 +440,21 @@ void WebExtensionPolicy::GetContentScripts(
   aScripts.AppendElements(mContentScripts);
 }
 
+bool WebExtensionPolicy::CanAccessContext(nsILoadContext* aContext) const {
+  MOZ_ASSERT(aContext);
+  return mPrivateBrowsingAllowed || !aContext->UsePrivateBrowsing();
+}
+
+bool WebExtensionPolicy::CanAccessWindow(nsPIDOMWindowOuter* aWindow) const {
+  if (mPrivateBrowsingAllowed) {
+    return true;
+  }
+  // match browsing mode with policy
+  nsIDocShell* docShell = aWindow->GetDocShell();
+  nsCOMPtr<nsILoadContext> loadContext = do_QueryInterface(docShell);
+  return !(loadContext && loadContext->UsePrivateBrowsing());
+}
+
 NS_IMPL_CYCLE_COLLECTION_WRAPPERCACHE(WebExtensionPolicy, mParent,
                                       mLocalizeCallback, mHostPermissions,
                                       mWebAccessiblePaths, mContentScripts)
@@ -545,6 +560,12 @@ bool MozDocumentMatcher::Matches(const DocInfo& aDoc) const {
     }
   }
 
+  // match browsing mode with policy
+  nsCOMPtr<nsILoadContext> loadContext = aDoc.GetLoadContext();
+  if (loadContext && mExtension && !mExtension->CanAccessContext(loadContext)) {
+    return false;
+  }
+
   if (!mMatchAboutBlank && aDoc.URL().InheritsPrincipal()) {
     return false;
   }
diff --git a/toolkit/components/extensions/WebExtensionPolicy.h b/toolkit/components/extensions/WebExtensionPolicy.h
index cca37baad0d2..f82a2643df5e 100644
--- a/toolkit/components/extensions/WebExtensionPolicy.h
+++ b/toolkit/components/extensions/WebExtensionPolicy.h
@@ -121,6 +121,15 @@ class WebExtensionPolicy final : public nsISupports,
   bool Active() const { return mActive; }
   void SetActive(bool aActive, ErrorResult& aRv);
 
+  bool PrivateBrowsingAllowed() const { return mPrivateBrowsingAllowed; }
+  void SetPrivateBrowsingAllowed(bool aPrivateBrowsingAllowed) {
+    mPrivateBrowsingAllowed = aPrivateBrowsingAllowed;
+  };
+
+  bool CanAccessContext(nsILoadContext* aContext) const;
+
+  bool CanAccessWindow(nsPIDOMWindowOuter* aWindow) const;
+
   static void GetActiveExtensions(
       dom::GlobalObject& aGlobal,
       nsTArray<RefPtr<WebExtensionPolicy>>& aResults);
@@ -173,6 +182,8 @@ class WebExtensionPolicy final : public nsISupports,
   RefPtr<MatchPatternSet> mHostPermissions;
   MatchGlobSet mWebAccessiblePaths;
 
+  bool mPrivateBrowsingAllowed = false;
+
   dom::Nullable<nsTArray<nsString>> mBackgroundScripts;
 
   nsTArray<RefPtr<WebExtensionContentScript>> mContentScripts;
diff --git a/toolkit/components/extensions/extension-process-script.js b/toolkit/components/extensions/extension-process-script.js
index 83fae9b16729..586ffe3f5574 100644
--- a/toolkit/components/extensions/extension-process-script.js
+++ b/toolkit/components/extensions/extension-process-script.js
@@ -145,6 +145,8 @@ ExtensionManager = {
         allowedOrigins: extension.whiteListedHosts,
         webAccessibleResources: extension.webAccessibleResources,
 
+        privateBrowsingAllowed: extension.privateBrowsingAllowed,
+
         contentSecurityPolicy: extension.contentSecurityPolicy,
 
         localizeCallback,
diff --git a/toolkit/components/extensions/parent/ext-extension.js b/toolkit/components/extensions/parent/ext-extension.js
index 7afc828d9564..a4b54c0eed7d 100644
--- a/toolkit/components/extensions/parent/ext-extension.js
+++ b/toolkit/components/extensions/parent/ext-extension.js
@@ -9,11 +9,11 @@ this.extension = class extends ExtensionAPI {
         },
 
         isAllowedIncognitoAccess() {
-          return Promise.resolve(true);
+          return context.privateBrowsingAllowed;
         },
 
         isAllowedFileSchemeAccess() {
-          return Promise.resolve(false);
+          return false;
         },
       },
     };
diff --git a/toolkit/components/extensions/schemas/manifest.json b/toolkit/components/extensions/schemas/manifest.json
index aef24b5e1074..10238018e401 100644
--- a/toolkit/components/extensions/schemas/manifest.json
+++ b/toolkit/components/extensions/schemas/manifest.json
@@ -102,8 +102,8 @@
           "incognito": {
             "type": "string",
             "enum": ["spanning"],
-            "optional": true,
-            "onError": "warn"
+            "default": "spanning",
+            "optional": true
           },
 
           "background": {
diff --git a/toolkit/components/extensions/test/xpcshell/test_ext_extension.js b/toolkit/components/extensions/test/xpcshell/test_ext_extension.js
index 97ca3c9ee488..5b9572db50a4 100644
--- a/toolkit/components/extensions/test/xpcshell/test_ext_extension.js
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_extension.js
@@ -12,7 +12,6 @@ add_task(async function test_is_allowed_incognito_access() {
 
   let extension = ExtensionTestUtils.loadExtension({
     background,
-    manifest: {},
   });
 
   await extension.startup();
@@ -20,6 +19,24 @@ add_task(async function test_is_allowed_incognito_access() {
   await extension.unload();
 });
 
+add_task(async function test_is_denied_incognito_access() {
+  async function background() {
+    let allowed = await browser.extension.isAllowedIncognitoAccess();
+
+    browser.test.assertEq(false, allowed, "isAllowedIncognitoAccess is false");
+    browser.test.notifyPass("isNotAllowedIncognitoAccess");
+  }
+
+  let extension = ExtensionTestUtils.loadExtension({
+    background,
+    incognitoOverride: "not_allowed",
+  });
+
+  await extension.startup();
+  await extension.awaitFinish("isNotAllowedIncognitoAccess");
+  await extension.unload();
+});
+
 add_task(async function test_in_incognito_context_false() {
   function background() {
     browser.test.assertEq(false, browser.extension.inIncognitoContext, "inIncognitoContext returned false");
@@ -28,7 +45,6 @@ add_task(async function test_in_incognito_context_false() {
 
   let extension = ExtensionTestUtils.loadExtension({
     background,
-    manifest: {},
   });
 
   await extension.startup();
@@ -46,7 +62,6 @@ add_task(async function test_is_allowed_file_scheme_access() {
 
   let extension = ExtensionTestUtils.loadExtension({
     background,
-    manifest: {},
   });
 
   await extension.startup();
diff --git a/toolkit/components/extensions/test/xpcshell/test_ext_incognito.js b/toolkit/components/extensions/test/xpcshell/test_ext_incognito.js
new file mode 100644
index 000000000000..947772f701cd
--- /dev/null
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_incognito.js
@@ -0,0 +1,30 @@
+/* -*- Mode: indent-tabs-mode: nil; js-indent-level: 2 -*- */
+/* vim: set sts=2 sw=2 et tw=80: */
+"use strict";
+
+add_task(async function test_extension_incognito_spanning() {
+  let wrapper = ExtensionTestUtils.loadExtension({});
+  await wrapper.startup();
+
+  let extension = wrapper.extension;
+  let data = extension.serialize();
+  equal(data.privateBrowsingAllowed, true, "Should have privateBrowsingAllowed in serialized extension");
+  equal(extension.privateBrowsingAllowed, true, "Should have privateBrowsingAllowed");
+  equal(extension.policy.privateBrowsingAllowed, true, "Should have privateBrowsingAllowed on policy");
+  await wrapper.unload();
+});
+
+// This tests setting an extension to private-only mode which is useful for testing.
+add_task(async function test_extension_incognito_test_mode() {
+  let wrapper = ExtensionTestUtils.loadExtension({
+    incognitoOverride: "not_allowed",
+  });
+  await wrapper.startup();
+
+  let extension = wrapper.extension;
+  let data = extension.serialize();
+  equal(data.privateBrowsingAllowed, false, "Should not have privateBrowsingAllowed in serialized extension");
+  equal(extension.privateBrowsingAllowed, false, "Should not have privateBrowsingAllowed");
+  equal(extension.policy.privateBrowsingAllowed, false, "Should not have privateBrowsingAllowed on policy");
+  await wrapper.unload();
+});
diff --git a/toolkit/components/extensions/test/xpcshell/test_ext_manifest_incognito.js b/toolkit/components/extensions/test/xpcshell/test_ext_manifest_incognito.js
index 12e07ad5af81..c8adcf864b63 100644
--- a/toolkit/components/extensions/test/xpcshell/test_ext_manifest_incognito.js
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_manifest_incognito.js
@@ -14,14 +14,25 @@ add_task(async function test_manifest_incognito() {
         "spanning",
         "Should have the expected incognito string");
 
+  normalized = await ExtensionTestUtils.normalizeManifest({
+    "incognito": "not_allowed",
+  });
+
+  equal(normalized.error,
+        'Error processing incognito: Invalid enumeration value "not_allowed"',
+        "Should have an error");
+  Assert.deepEqual(normalized.errors, [], "Should not have a warning");
+  equal(normalized.value, undefined,
+        "Invalid incognito string should be undefined");
+
   normalized = await ExtensionTestUtils.normalizeManifest({
     "incognito": "split",
   });
 
-  equal(normalized.error, undefined, "Should not have an error");
-  Assert.deepEqual(normalized.errors,
-                   ['Error processing incognito: Invalid enumeration value "split"'],
-                   "Should have the expected warning");
-  equal(normalized.value.incognito, null,
-        "Invalid incognito string should be omitted");
+  equal(normalized.error,
+        'Error processing incognito: Invalid enumeration value "split"',
+        "Should have an error");
+  Assert.deepEqual(normalized.errors, [], "Should not have a warning");
+  equal(normalized.value, undefined,
+        "Invalid incognito string should be undefined");
 });
diff --git a/toolkit/components/extensions/test/xpcshell/xpcshell-common.ini b/toolkit/components/extensions/test/xpcshell/xpcshell-common.ini
index 8b013bb42947..b5742483adb4 100644
--- a/toolkit/components/extensions/test/xpcshell/xpcshell-common.ini
+++ b/toolkit/components/extensions/test/xpcshell/xpcshell-common.ini
@@ -60,6 +60,7 @@ skip-if = os == "android" # checking for telemetry needs to be updated: 1384923
 [test_ext_extension_startup_telemetry.js]
 [test_ext_geturl.js]
 [test_ext_idle.js]
+[test_ext_incognito.js]
 [test_ext_localStorage.js]
 [test_ext_management.js]
 skip-if = (os == "win" && !debug) #Bug 1419183 disable on Windows