diff --git a/toolkit/components/extensions/ext-c-runtime.js b/toolkit/components/extensions/ext-c-runtime.js
index 8991034e6c3e..192d3c5aec91 100644
--- a/toolkit/components/extensions/ext-c-runtime.js
+++ b/toolkit/components/extensions/ext-c-runtime.js
@@ -24,6 +24,7 @@ this.runtime = class extends ExtensionAPI {
 
         sendMessage(...args) {
           let extensionId, message, options, responseCallback;
+
           if (typeof args[args.length - 1] === "function") {
             responseCallback = args.pop();
           }
@@ -55,18 +56,18 @@ this.runtime = class extends ExtensionAPI {
             message = args[0];
           } else if (args.length === 2) {
             // With two optional arguments, this is the ambiguous case,
-            // particularly sendMessage("string", {});
+            // particularly sendMessage("string", {} or null)
             // Given that sending a message within the extension is generally
             // more common than sending the empty object to another extension,
             // we prefer that conclusion, as long as the second argument looks
-            // like valid options.
+            // like valid options object, or is null/undefined.
             let [validOpts] = checkOptions(args[1]);
-            if (validOpts) {
+            if (validOpts || args[1] == null) {
               [message, options] = args;
             } else {
               [extensionId, message] = args;
             }
-          } else if (args.length === 3) {
+          } else if (args.length === 3 || (args.length === 4 && args[3] == null)) {
             [extensionId, message, options] = args;
           } else if (args.length === 4 && !responseCallback) {
             return Promise.reject({message: "runtime.sendMessage's last argument is not a function"});
diff --git a/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_args.js b/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_args.js
index d2bb437b6362..5134f71117e6 100644
--- a/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_args.js
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_args.js
@@ -59,6 +59,10 @@ add_task(async function() {
   // Due to this insane design we parse its arguments manually.  This
   // test is meant to cover all the combinations.
 
+  // A single null or undefined argument is allowed, and represents the message
+  extension1.sendMessage(null);
+  await checkLocalMessage(null);
+
   // With one argument, it must be just the message
   extension1.sendMessage("message");
   await checkLocalMessage("message");
@@ -70,13 +74,25 @@ add_task(async function() {
   extension1.sendMessage(ID2, {msg: "message"});
   await checkRemoteMessage({msg: "message"});
 
-  // And this case should be (message, options)
+  // And these should be (message, options)
   extension1.sendMessage("message", {});
   await checkLocalMessage("message");
 
+  // or (message, non-callback), pick your poison
+  extension1.sendMessage("message", undefined);
+  await checkLocalMessage("message");
+
   // With three arguments, we send a cross-extension message
   extension1.sendMessage(ID2, "message", {});
   await checkRemoteMessage("message");
 
+  // Even when the last one is null or undefined
+  extension1.sendMessage(ID2, "message", undefined);
+  await checkRemoteMessage("message");
+
+  // The four params case is unambigous, so we allow null as a (non-) callback
+  extension1.sendMessage(ID2, "message", {}, null);
+  await checkRemoteMessage("message");
+
   await Promise.all([extension1.unload(), extension2.unload()]);
 });
diff --git a/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_errors.js b/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_errors.js
index 9b0e00de7f41..cc60ff6622ab 100644
--- a/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_errors.js
+++ b/toolkit/components/extensions/test/xpcshell/test_ext_runtime_sendMessage_errors.js
@@ -9,7 +9,7 @@ add_task(async function test_sendMessage_error() {
     let testCases = [
       // [arguments, expected error string],
       [[], "runtime.sendMessage's message argument is missing"],
-      [[null, null, null, null], "runtime.sendMessage's last argument is not a function"],
+      [[null, null, null, 42], "runtime.sendMessage's last argument is not a function"],
       [[null, null, 1], "runtime.sendMessage's options argument is invalid"],
       [[1, null, null], "runtime.sendMessage's extensionId argument is invalid"],
       [[null, null, null, null, null], "runtime.sendMessage received too many arguments"],