diff --git a/mail/app/profile/all-thunderbird.js b/mail/app/profile/all-thunderbird.js
index 169a7bb20e..9d7dc58abd 100644
--- a/mail/app/profile/all-thunderbird.js
+++ b/mail/app/profile/all-thunderbird.js
@@ -173,6 +173,11 @@ pref("extensions.overlayloader.loglevel", "warn");
 
 pref("extensions.abuseReport.enabled", false);
 
+// Delay opening of action popups until the browser is fully loaded.
+// This is needed on Wayland systems, but can be enabled for other
+// systems for debug purposes as well. See Bug 1905622.
+pref("extensions.openPopupDelayedFullyLoaded.enabled", false);
+
 // Strict compatibility makes add-ons incompatible by default.
 #ifndef RELEASE_OR_BETA
 pref("extensions.strictCompatibility", false);
diff --git a/mail/components/extensions/ExtensionPopups.sys.mjs b/mail/components/extensions/ExtensionPopups.sys.mjs
index 801d1afea1..8052807380 100644
--- a/mail/components/extensions/ExtensionPopups.sys.mjs
+++ b/mail/components/extensions/ExtensionPopups.sys.mjs
@@ -44,6 +44,7 @@ export class BasePopup {
     this.contentReady = new Promise(resolve => {
       this._resolveContentReady = resolve;
     });
+    this.contentReadyAndResized = Promise.withResolvers();
 
     this.window.addEventListener("unload", this);
     this.viewNode.addEventListener("popuphiding", this);
@@ -160,6 +161,10 @@ export class BasePopup {
 
       case "Extension:BrowserResized":
         this._resolveContentReady();
+        // The final resize is marked as delayed, which is the one we have to wait for.
+        if (data.detail == "delayed") {
+          this.contentReadyAndResized.resolve();
+        }
         if (this.ignoreResizes) {
           this.dimensions = data;
         } else {
diff --git a/mail/components/extensions/ExtensionToolbarButtons.sys.mjs b/mail/components/extensions/ExtensionToolbarButtons.sys.mjs
index e2131dcdf4..86396604da 100644
--- a/mail/components/extensions/ExtensionToolbarButtons.sys.mjs
+++ b/mail/components/extensions/ExtensionToolbarButtons.sys.mjs
@@ -493,6 +493,19 @@ export class ToolbarButtonAPI extends ExtensionAPIPersistent {
         const popup =
           lazy.ViewPopup.for(this.extension, window.top) ||
           this.getPopup(window.top, popupURL);
+
+        // Bug 1905622: We have to delay opening the panel, until after its browser
+        // has been loaded, otherwise the content will be blank.
+        if (
+          popup.viewNode.isWaylandPopup ||
+          Services.prefs.getBoolPref(
+            "extensions.openPopupDelayedFullyLoaded.enabled"
+          )
+        ) {
+          await popup.browserLoaded;
+          await popup.contentReadyAndResized.promise;
+        }
+
         popup.viewNode.openPopup(button, "bottomleft topleft", 0, 0);
       } else if (!options.requirePopupUrl) {
         if (!this.lastClickInfo) {