diff --git a/devtools/client/inspector/inspector.js b/devtools/client/inspector/inspector.js
index 4c38f413b7d8..b9430937e153 100644
--- a/devtools/client/inspector/inspector.js
+++ b/devtools/client/inspector/inspector.js
@@ -1302,7 +1302,11 @@ Inspector.prototype = {
   onResourceAvailable: function(resources) {
     for (const resource of resources) {
       if (
-        resource.resourceType === this.toolbox.resourceWatcher.TYPES.ROOT_NODE
+        resource.resourceType ===
+          this.toolbox.resourceWatcher.TYPES.ROOT_NODE &&
+        // It might happen that the ROOT_NODE resource (which is a Front) is already
+        // destroyed, and in such case we want to ignore it.
+        !resource.isDestroyed()
       ) {
         const rootNodeFront = resource;
         const isTopLevelTarget = !!resource.targetFront.isTopLevel;
diff --git a/devtools/client/inspector/markup/markup.js b/devtools/client/inspector/markup/markup.js
index 1e117d26f01b..be3e0877979a 100644
--- a/devtools/client/inspector/markup/markup.js
+++ b/devtools/client/inspector/markup/markup.js
@@ -1442,8 +1442,11 @@ MarkupView.prototype = {
 
   _onResourceAvailable: async function(resources) {
     for (const resource of resources) {
-      if (resource.resourceType !== this.resourceWatcher.TYPES.ROOT_NODE) {
-        // Only handle root-node resources
+      if (
+        resource.resourceType !== this.resourceWatcher.TYPES.ROOT_NODE ||
+        resource.isDestroyed()
+      ) {
+        // Only handle alive root-node resources
         continue;
       }
 
diff --git a/devtools/client/inspector/shared/highlighters-overlay.js b/devtools/client/inspector/shared/highlighters-overlay.js
index 161bfd4da063..9aa50b3ceaad 100644
--- a/devtools/client/inspector/shared/highlighters-overlay.js
+++ b/devtools/client/inspector/shared/highlighters-overlay.js
@@ -1741,7 +1741,12 @@ class HighlightersOverlay {
    */
   async _onResourceAvailable(resources) {
     for (const resource of resources) {
-      if (resource.resourceType !== this.resourceWatcher.TYPES.ROOT_NODE) {
+      if (
+        resource.resourceType !== this.resourceWatcher.TYPES.ROOT_NODE ||
+        // It might happen that the ROOT_NODE resource (which is a Front) is already
+        // destroyed, and in such case we want to ignore it.
+        resource.isDestroyed()
+      ) {
         // Only handle root-node resources.
         // Note that we could replace this with DOCUMENT_EVENT resources, since
         // the actual root-node resource is not used here.