diff --git a/src/ProjectTemplates/Shared/AspNetProcess.cs b/src/ProjectTemplates/Shared/AspNetProcess.cs
index e5fa728290..fe0f05fd7a 100644
--- a/src/ProjectTemplates/Shared/AspNetProcess.cs
+++ b/src/ProjectTemplates/Shared/AspNetProcess.cs
@@ -44,7 +44,7 @@ namespace Templates.Test.Helpers
             string workingDirectory,
             string dllPath,
             IDictionary<string, string> environmentVariables,
-            bool published = true,
+            bool published,
             bool hasListeningUri = true,
             ILogger logger = null)
         {
diff --git a/src/ProjectTemplates/Shared/Project.cs b/src/ProjectTemplates/Shared/Project.cs
index 1fa0b57a26..6eae96dce0 100644
--- a/src/ProjectTemplates/Shared/Project.cs
+++ b/src/ProjectTemplates/Shared/Project.cs
@@ -147,8 +147,33 @@ namespace Templates.Test.Helpers
                 ["ASPNETCORE_Logging__Console__IncludeScopes"] = "true",
             };
 
+            var launchSettingsJson = Path.Combine(TemplateOutputDir, "Properties", "launchSettings.json");
+            if (File.Exists(launchSettingsJson))
+            {
+                // When executing "dotnet run", the launch urls specified in the app's launchSettings.json have higher precedence
+                // than ambient environment variables. When present, we have to edit this file to allow the application to pick random ports.
+                var original = File.ReadAllText(launchSettingsJson);
+                var updated = original.Replace(
+                    "\"applicationUrl\": \"https://localhost:5001;http://localhost:5000\"",
+                    $"\"applicationUrl\": \"{_urls}\"");
+
+                if (updated == original)
+                {
+                    Output.WriteLine("applicationUrl is not specified in launchSettings.json");
+                }
+                else
+                {
+                    Output.WriteLine("Updating applicationUrl in launchSettings.json");
+                    File.WriteAllText(launchSettingsJson, updated);
+                }
+            }
+            else
+            {
+                Output.WriteLine("No launchSettings.json found to update.");
+            }
+
             var projectDll = Path.Combine(TemplateBuildDir, $"{ProjectName}.dll");
-            return new AspNetProcess(Output, TemplateOutputDir, projectDll, environment, hasListeningUri: hasListeningUri, logger: logger);
+            return new AspNetProcess(Output, TemplateOutputDir, projectDll, environment, published: false, hasListeningUri: hasListeningUri, logger: logger);
         }
 
         internal AspNetProcess StartPublishedProjectAsync(bool hasListeningUri = true)
@@ -163,7 +188,7 @@ namespace Templates.Test.Helpers
             };
 
             var projectDll = $"{ProjectName}.dll";
-            return new AspNetProcess(Output, TemplatePublishDir, projectDll, environment, hasListeningUri: hasListeningUri);
+            return new AspNetProcess(Output, TemplatePublishDir, projectDll, environment, published: true, hasListeningUri: hasListeningUri);
         }
 
         internal async Task<ProcessResult> RunDotNetEfCreateMigrationAsync(string migrationName)