diff --git a/devtools/client/shared/test/test-actor-registry.js b/devtools/client/shared/test/test-actor-registry.js
index 1e71a26ce578..fa23f6a5e363 100644
--- a/devtools/client/shared/test/test-actor-registry.js
+++ b/devtools/client/shared/test/test-actor-registry.js
@@ -65,6 +65,11 @@
 
     await client.connect();
 
+    // Force connecting to the tab so that the actor is registered in the tab.
+    // Calling `getTab` will spawn a DebuggerServer and ActorRegistry in the content
+    // process.
+    await client.mainRoot.getTab({tab});
+
     // We also need to make sure the test actor is registered on the server.
     await exports.registerTestActor(client);
 
diff --git a/devtools/client/webide/test/test_autoconnect_runtime.html b/devtools/client/webide/test/test_autoconnect_runtime.html
index 1c8f6c20ab69..f708d3804f5b 100644
--- a/devtools/client/webide/test/test_autoconnect_runtime.html
+++ b/devtools/client/webide/test/test_autoconnect_runtime.html
@@ -67,6 +67,10 @@
           await connectionsChanged;
           is(Object.keys(DebuggerServer._connections).length, 0, "Disconnected");
 
+          // The DebuggerServer is destroyed when closing WebIDE, so re-initialize it.
+          DebuggerServer.init();
+          DebuggerServer.registerAllActors();
+
           connectionsChanged = waitForConnectionChange("opened", 2);
 
           win = await openWebIDE();
diff --git a/devtools/client/webide/test/test_autoselect_project.html b/devtools/client/webide/test/test_autoselect_project.html
index 1e57c9534b1d..4bdfa38bcc5f 100644
--- a/devtools/client/webide/test/test_autoselect_project.html
+++ b/devtools/client/webide/test/test_autoselect_project.html
@@ -61,6 +61,10 @@
           await connectionsChanged;
           is(Object.keys(DebuggerServer._connections).length, 0, "Disconnected");
 
+          // The DebuggerServer is destroyed when closing WebIDE, so re-initialize it.
+          DebuggerServer.init();
+          DebuggerServer.registerAllActors();
+
           connectionsChanged = waitForConnectionChange("opened", 2);
 
           // Re-open, should reselect main process after connection
diff --git a/devtools/server/startup/frame.js b/devtools/server/startup/frame.js
index 6f466f0339ee..c7e06e20a17a 100644
--- a/devtools/server/startup/frame.js
+++ b/devtools/server/startup/frame.js
@@ -122,6 +122,19 @@ try {
       }
       connections.clear();
     });
+
+    // Destroy the server once its last connection closes. Note that multiple frame
+    // scripts may be running in parallel and reuse the same server.
+    function destroyServer() {
+      // Only destroy the server if there is no more connections to it. It may be used
+      // to debug another tab running in the same process.
+      if (DebuggerServer.hasConnection()) {
+        return;
+      }
+      DebuggerServer.off("connectionchange", destroyServer);
+      DebuggerServer.destroy();
+    }
+    DebuggerServer.on("connectionchange", destroyServer);
   })();
 } catch (e) {
   dump(`Exception in DevTools frame startup: ${e}\n`);
diff --git a/devtools/server/tests/browser/browser.ini b/devtools/server/tests/browser/browser.ini
index 6cb65d02b5ce..af4fe1d76ec7 100644
--- a/devtools/server/tests/browser/browser.ini
+++ b/devtools/server/tests/browser/browser.ini
@@ -72,6 +72,7 @@ skip-if = e10s # Bug 1183605 - devtools/server/tests/browser/ tests are still di
 skip-if = e10s # Bug 1183605 - devtools/server/tests/browser/ tests are still disabled in E10S
 [browser_canvasframe_helper_06.js]
 skip-if = e10s # Bug 1183605 - devtools/server/tests/browser/ tests are still disabled in E10S
+[browser_debugger_server.js]
 [browser_inspector-anonymous.js]
 [browser_inspector-insert.js]
 [browser_inspector-mutations-childlist.js]
diff --git a/devtools/server/tests/browser/browser_debugger_server.js b/devtools/server/tests/browser/browser_debugger_server.js
new file mode 100644
index 000000000000..9e7d368e5726
--- /dev/null
+++ b/devtools/server/tests/browser/browser_debugger_server.js
@@ -0,0 +1,59 @@
+/* vim: set ft=javascript ts=2 et sw=2 tw=80: */
+/* Any copyright is dedicated to the Public Domain.
+   http://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+// Test basic features of DebuggerServer
+
+add_task(async function() {
+  // When running some other tests before, they may not destroy the main server.
+  // Do it manually before running our tests.
+  if (DebuggerServer.initialized) {
+    DebuggerServer.destroy();
+  }
+
+  await testDebuggerServerInitialized();
+});
+
+async function testDebuggerServerInitialized() {
+  const browser = await addTab("data:text/html;charset=utf-8,foo");
+  const tab = gBrowser.getTabForBrowser(browser);
+
+  ok(!DebuggerServer.initialized,
+    "By default, the DebuggerServer isn't initialized in parent process");
+  await ContentTask.spawn(browser, null, function() {
+    const {require} = ChromeUtils.import("resource://devtools/shared/Loader.jsm", {});
+    const {DebuggerServer} = require("devtools/server/main");
+    ok(!DebuggerServer.initialized,
+      "By default, the DebuggerServer isn't initialized not in content process");
+  });
+
+  const target = await TargetFactory.forTab(tab);
+
+  ok(DebuggerServer.initialized,
+    "TargetFactory.forTab will initialize the DebuggerServer in parent process");
+  await ContentTask.spawn(browser, null, function() {
+    const {require} = ChromeUtils.import("resource://devtools/shared/Loader.jsm", {});
+    const {DebuggerServer} = require("devtools/server/main");
+    ok(DebuggerServer.initialized,
+      "TargetFactory.forTab will initialize the DebuggerServer in content process");
+  });
+
+  await target.destroy();
+
+  // Disconnecting the client will remove all connections from both server,
+  // in parent and content process. But only the one in the content process will be
+  // destroyed.
+  ok(DebuggerServer.initialized,
+    "Destroying the target doesn't destroy the DebuggerServer in the parent process");
+  await ContentTask.spawn(browser, null, function() {
+    const {require} = ChromeUtils.import("resource://devtools/shared/Loader.jsm", {});
+    const {DebuggerServer} = require("devtools/server/main");
+    ok(!DebuggerServer.initialized,
+      "But destroying the target ends up destroying the DebuggerServer in the content" +
+      " process");
+  });
+
+  gBrowser.removeCurrentTab();
+}
diff --git a/devtools/server/tests/mochitest/test_connectToFrame.html b/devtools/server/tests/mochitest/test_connectToFrame.html
index 057f7c70c7a7..3221fca45d58 100644
--- a/devtools/server/tests/mochitest/test_connectToFrame.html
+++ b/devtools/server/tests/mochitest/test_connectToFrame.html
@@ -80,47 +80,60 @@ function runTests() {
     DebuggerServer.registerAllActors();
   }
 
-  function firstClient() {
+  async function firstClient() {
     // Fake a first connection to an iframe
     const transport = DebuggerServer.connectPipe();
     const conn = transport._serverConnection;
     const client = new DebuggerClient(transport);
-    DebuggerServer.connectToFrame(conn, iframe).then(actor => {
-      ok(actor.testActor, "Got the test actor");
+    const actor = await DebuggerServer.connectToFrame(conn, iframe);
+    ok(actor.testActor, "Got the test actor");
 
-      // Ensure sending at least one request to our actor,
-      // otherwise it won't be instantiated, nor be destroyed...
-      client.request({
-        to: actor.testActor,
-        type: "hello",
-      }, function(response) {
-        // Then close the client. That should end up cleaning our test actor
-        client.close();
+    // Ensure sending at least one request to our actor,
+    // otherwise it won't be instantiated, nor be destroyed...
+    await client.request({
+      to: actor.testActor,
+      type: "hello",
+    });
 
-        // Ensure that our test actor got cleaned up;
-        // its destroy method should be called
-        mm.addMessageListener("test-actor-destroyed", function listener() {
-          mm.removeMessageListener("test-actor-destroyed", listener);
-          ok(true, "Actor is cleaned up");
+    // Connect a second client in parallel to asser that it received a distinct set of
+    // target actors
+    await secondClient(actor.testActor);
 
-          secondClient(actor.testActor);
-        });
+    ok(DebuggerServer.initialized,
+      "DebuggerServer isn't destroyed until all clients are disconnected");
+
+    // Ensure that our test actor got cleaned up;
+    // its destroy method should be called
+    const onActorDestroyed = new Promise(resolve => {
+      mm.addMessageListener("test-actor-destroyed", function listener() {
+        mm.removeMessageListener("test-actor-destroyed", listener);
+        ok(true, "Actor is cleaned up");
+        resolve();
       });
     });
+
+    // Then close the client. That should end up cleaning our test actor
+    await client.close();
+
+    await onActorDestroyed;
+
+    // This test loads a frame in the parent process, so that we end up sharing the same
+    // DebuggerServer instance
+    ok(!DebuggerServer.initialized,
+      "DebuggerServer is destroyed when all clients are disconnected");
+    cleanup();
   }
 
-  function secondClient(firstActor) {
+  async function secondClient(firstActor) {
     // Then fake a second one, that should spawn a new set of target-scoped actors
     const transport = DebuggerServer.connectPipe();
     const conn = transport._serverConnection;
     const client = new DebuggerClient(transport);
-    DebuggerServer.connectToFrame(conn, iframe).then(actor => {
-      ok(actor.testActor, "Got a test actor for the second connection");
-      isnot(actor.testActor, firstActor,
-            "We get different actor instances between two connections");
-
-      client.close(cleanup);
-    });
+    const actor = await DebuggerServer.connectToFrame(conn, iframe);
+    ok(actor.testActor, "Got a test actor for the second connection");
+    isnot(actor.testActor, firstActor,
+          "We get different actor instances between two connections");
+    return client.close();
   }
 
   function cleanup() {