diff --git a/src/DynamoCoreWpf/ViewModels/Core/DynamoViewModel.cs b/src/DynamoCoreWpf/ViewModels/Core/DynamoViewModel.cs
index 2fbe44f1901..29f61fd54ca 100644
--- a/src/DynamoCoreWpf/ViewModels/Core/DynamoViewModel.cs
+++ b/src/DynamoCoreWpf/ViewModels/Core/DynamoViewModel.cs
@@ -2180,6 +2180,18 @@ private void OpenFromJson(object parameters)
             this.ShowStartPage = false; // Hide start page if there's one.
         }
 
+        /// <summary>
+        /// Resets trust warning state when a preemptively shown popup should be dismissed.
+        /// </summary>
+        /// <param name="trustWarningWasShown">True when this open/insert flow displayed the trust warning before command execution.</param>
+        private void ResetTrustWarningStateIfNeeded(bool trustWarningWasShown)
+        {
+            if (!trustWarningWasShown || FileTrustViewModel == null) return;
+
+            FileTrustViewModel.ShowWarningPopup = false;
+            RunSettings.ForceBlockRun = false;
+        }
+
         /// <summary>
         /// Open a definition or workspace.
         /// For most cases, parameters variable refers to the file path to open
@@ -2203,6 +2215,7 @@ private void Open(object parameters)
             fileContents = string.Empty;
             bool forceManualMode = false;
             bool isTemplate = false;
+            bool trustWarningWasShown = false;
             try
             {
                 if (parameters is Tuple<string, bool> packedParams)
@@ -2229,25 +2242,33 @@ private void Open(object parameters)
                     && !DynamoModel.IsTestMode
                     && !PreferenceSettings.DisableTrustWarnings
                     && FileTrustViewModel != null;
-                RunSettings.ForceBlockRun = displayTrustWarning;
-                // Execute graph open command
-                ExecuteCommand(new DynamoModel.OpenFileCommand(filePath, forceManualMode, isTemplate));
 
-                // Apply annotation updates based on the preference setting
-                RefreshAnnotationDescriptions();
-
-                // Only show trust warning popop when current opened workspace is homeworkspace and not custom node workspace
-                if (displayTrustWarning && (currentWorkspaceViewModel?.IsHomeSpace ?? false))
+                if (displayTrustWarning)
                 {
-                    // Skip these when opening dyf
                     FileTrustViewModel.AllowOneTimeTrust = false;
                     FileTrustViewModel.DynFileDirectoryName = directoryName;
                     FileTrustViewModel.ShowWarningPopup = true;
                     (HomeSpaceViewModel as HomeWorkspaceViewModel)?.UpdateRunStatusMsgBasedOnStates();
+                    trustWarningWasShown = true;
+                }
+
+                RunSettings.ForceBlockRun = displayTrustWarning;
+                // Execute graph open command
+                ExecuteCommand(new DynamoModel.OpenFileCommand(filePath, forceManualMode, isTemplate));
+
+                if (trustWarningWasShown)
+                {
+                    // Hide the preemptively shown popup if trust is now satisfied (trusted path or warnings disabled).
+                    ShowHideFileTrustWarningIfCurrentWorkspaceTrusted();
                 }
+
+                // Apply annotation updates based on the preference setting
+                RefreshAnnotationDescriptions();
             }
             catch (Exception e)
             {
+                ResetTrustWarningStateIfNeeded(trustWarningWasShown);
+
                 if (!DynamoModel.IsTestMode)
                 {
                     string commandString = String.Format(Resources.MessageErrorOpeningFileGeneral);
@@ -2301,6 +2322,7 @@ private void Insert(object parameters)
             filePath = string.Empty;
             fileContents = string.Empty;
             bool forceManualMode = true;
+            bool trustWarningWasShown = false;
             try
             {
                 if (parameters is Tuple<string, bool> packedParams)
@@ -2321,24 +2343,30 @@ private void Insert(object parameters)
                     && !DynamoModel.IsTestMode
                     && !PreferenceSettings.DisableTrustWarnings
                     && FileTrustViewModel != null;
-                RunSettings.ForceBlockRun = displayTrustWarning;
-                // Execute graph open command
-                ExecuteCommand(new DynamoModel.InsertFileCommand(filePath, forceManualMode));
-
-                this.FitViewCommand.Execute(null);
 
-                // Only show trust warning popup when current opened workspace is homeworkspace and not custom node workspace
-                if (displayTrustWarning && (currentWorkspaceViewModel?.IsHomeSpace ?? false))
+                if (displayTrustWarning)
                 {
-                    // Skip these when opening dyf
                     FileTrustViewModel.AllowOneTimeTrust = false;
                     FileTrustViewModel.DynFileDirectoryName = directoryName;
                     FileTrustViewModel.ShowWarningPopup = true;
                     (HomeSpaceViewModel as HomeWorkspaceViewModel)?.UpdateRunStatusMsgBasedOnStates();
+                    trustWarningWasShown = true;
+                }
+
+                RunSettings.ForceBlockRun = displayTrustWarning;
+                // Execute graph open command
+                ExecuteCommand(new DynamoModel.InsertFileCommand(filePath, forceManualMode));
+
+                this.FitViewCommand.Execute(null);
+                if (trustWarningWasShown)
+                {
+                    ShowHideFileTrustWarningIfCurrentWorkspaceTrusted();
                 }
             }
             catch (Exception e)
             {
+                ResetTrustWarningStateIfNeeded(trustWarningWasShown);
+
                 if (!DynamoModel.IsTestMode)
                 {
                     string commandString = String.Format(Resources.MessageErrorOpeningFileGeneral);
diff --git a/test/DynamoCoreWpfTests/DynamoViewTests.cs b/test/DynamoCoreWpfTests/DynamoViewTests.cs
index 030edfefbcd..ba704d70f79 100644
--- a/test/DynamoCoreWpfTests/DynamoViewTests.cs
+++ b/test/DynamoCoreWpfTests/DynamoViewTests.cs
@@ -106,6 +106,66 @@ public void OpeningWorkspaceWithTclsrustWarning()
             DynamoModel.IsTestMode = true;
         }
 
+        [Test]
+        public void WhenOpeningWorkspaceThenTrustWarningIsShownBeforeCommand()
+        {
+            DynamoModel.IsTestMode = false;
+            bool? popupStateWhenOpenStarts = null;
+
+            void OnCommandStarting(DynamoModel.RecordableCommand command)
+            {
+                if (command is DynamoModel.OpenFileCommand)
+                {
+                    popupStateWhenOpenStarts = ViewModel.FileTrustViewModel.ShowWarningPopup;
+                }
+            }
+
+            Model.CommandStarting += OnCommandStarting;
+            try
+            {
+                Open(@"core\CustomNodes\TestAdd.dyn");
+            }
+            finally
+            {
+                Model.CommandStarting -= OnCommandStarting;
+                DynamoModel.IsTestMode = true;
+            }
+
+            Assert.IsTrue(popupStateWhenOpenStarts.GetValueOrDefault(false));
+        }
+
+        [Test]
+        public void WhenInsertingWorkspaceThenTrustWarningIsShownBeforeCommand()
+        {
+            DynamoModel.IsTestMode = false;
+            bool? popupStateWhenInsertStarts = null;
+
+            void OnCommandStarting(DynamoModel.RecordableCommand command)
+            {
+                if (command is DynamoModel.InsertFileCommand)
+                {
+                    popupStateWhenInsertStarts = ViewModel.FileTrustViewModel.ShowWarningPopup;
+                }
+            }
+
+            Model.CommandStarting += OnCommandStarting;
+            try
+            {
+                var insertMethod = typeof(DynamoViewModel).GetMethod("Insert", BindingFlags.NonPublic | BindingFlags.Instance);
+                Assert.NotNull(insertMethod);
+
+                var insertPath = Path.Combine(GetTestDirectory(ExecutingDirectory), @"core\CustomNodes\TestAdd.dyn");
+                insertMethod.Invoke(ViewModel, new object[] { insertPath });
+            }
+            finally
+            {
+                Model.CommandStarting -= OnCommandStarting;
+                DynamoModel.IsTestMode = true;
+            }
+
+            Assert.IsTrue(popupStateWhenInsertStarts.GetValueOrDefault(false));
+        }
+
         [Test]
         public void TestHomeWorkspaceClosedBeforeCustomNode()
         {