diff --git a/src/ProjectTemplates/Web.ProjectTemplates/WebApiAot-CSharp.csproj.in b/src/ProjectTemplates/Web.ProjectTemplates/WebApiAot-CSharp.csproj.in
index 135250791270..9445c03a87bd 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/WebApiAot-CSharp.csproj.in
+++ b/src/ProjectTemplates/Web.ProjectTemplates/WebApiAot-CSharp.csproj.in
@@ -10,4 +10,10 @@
     <PublishAot>true</PublishAot>
   </PropertyGroup>
 
+  <!--#if (EnableOpenAPI) -->
+  <ItemGroup>
+    <PackageReference Include="Microsoft.AspNetCore.OpenApi" Version="${MicrosoftAspNetCoreOpenApiVersion}" Condition="'$(EnableOpenAPI)' == 'True'" />
+  </ItemGroup>
+  <!--#endif -->
+
 </Project>
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/dotnetcli.host.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/dotnetcli.host.json
index 2569634c24f9..d24ccc689f1c 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/dotnetcli.host.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/dotnetcli.host.json
@@ -21,9 +21,13 @@
     "UseProgramMain": {
       "longName": "use-program-main",
       "shortName": ""
+    },
+    "DisableOpenAPI": {
+      "longName": "no-openapi",
+      "shortName": ""
     }
   },
   "usageExamples": [
     ""
   ]
-}
+}
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/ide.host.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/ide.host.json
index 00b1829bfeb4..de0bfb10ae91 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/ide.host.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/ide.host.json
@@ -9,6 +9,21 @@
       "isVisible": true,
       "persistenceScope": "shared",
       "persistenceScopeName": "Microsoft"
+    },
+    {
+      "id": "DisableOpenAPI",
+      "name": {
+        "text": "Enable _OpenAPI support",
+        "overrideDefaultText": true
+      },
+      "description": {
+        "text": "Enables OpenAPI (Swagger) support",
+        "overrideDefaultText": true
+      },
+      "invertBoolean": true,
+      "isVisible": true,
+      "defaultValue": "true",
+      "persistenceScope": "templateGroup"
     }
   ]
-}
+}
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.cs.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.cs.json
index d9f5aba08d8d..1fa10bab25ad 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.cs.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.cs.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Pokud se tato možnost zadá, přeskočí automatické obnovení projektu při vytvoření.",
   "symbols/UseProgramMain/displayName": "Nepoužívat _příkazy nejvyšší úrovně",
   "symbols/UseProgramMain/description": "Určuje, jestli se má místo příkazů nejvyšší úrovně generovat explicitní třída Program a metoda Main.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Obnoví balíčky NuGet vyžadované tímto projektem.",
   "postActions/restore/manualInstructions/default/text": "Spustit dotnet restore"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.de.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.de.json
index 82c0bf5121ef..72c37fdff835 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.de.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.de.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Wenn angegeben, wird die automatische Wiederherstellung des Projekts beim Erstellen übersprungen.",
   "symbols/UseProgramMain/displayName": "Keine Anweisungen_der obersten Ebene verwenden",
   "symbols/UseProgramMain/description": "Gibt an, ob anstelle von Anweisungen der obersten Ebene eine explizite Programmklasse und eine Main-Methode generiert werden soll.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "„NuGet-Pakete“ wiederherstellen, die für dieses Projekt erforderlich sind.",
   "postActions/restore/manualInstructions/default/text": "„dotnet restore“ ausführen"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.en.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.en.json
index 0805132c3eb8..1507b1e8498f 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.en.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.en.json
@@ -1,7 +1,7 @@
 {
   "author": "Microsoft",
   "name": "ASP.NET Core Web API (native AOT)",
-  "description": "A project template for creating a RESTful Web API using ASP.NET Core minimal APIs published as native AOT.",
+  "description": "A project template for creating a RESTful Web API using ASP.NET Core minimal APIs published as native AOT, with optional support for OpenAPI.",
   "symbols/ExcludeLaunchSettings/description": "Whether to exclude launchSettings.json from the generated template.",
   "symbols/kestrelHttpPort/description": "Port number to use for the HTTP endpoint in launchSettings.json.",
   "symbols/iisHttpPort/description": "Port number to use for the IIS Express HTTP endpoint in launchSettings.json.",
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "If specified, skips the automatic restore of the project on create.",
   "symbols/UseProgramMain/displayName": "Do not use _top-level statements",
   "symbols/UseProgramMain/description": "Whether to generate an explicit Program class and Main method instead of top-level statements.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Restore NuGet packages required by this project.",
   "postActions/restore/manualInstructions/default/text": "Run 'dotnet restore'"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.es.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.es.json
index 538c473b54a8..d6902478a520 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.es.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.es.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Si se especifica, se omite la restauración automática del proyecto durante la creación.",
   "symbols/UseProgramMain/displayName": "No usar instrucciones de _nivel superior",
   "symbols/UseProgramMain/description": "Indica si se debe generar una clase Program explícita y un método Main en lugar de instrucciones de nivel superior.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Restaure los paquetes NuGet necesarios para este proyecto.",
   "postActions/restore/manualInstructions/default/text": "Ejecutar \"dotnet restore\""
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.fr.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.fr.json
index 463429e219a1..5a6146402f37 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.fr.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.fr.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "S’il est spécifié, ignore la restauration automatique du projet lors de la création.",
   "symbols/UseProgramMain/displayName": "N’utilisez pas _d’instructions de niveau supérieur.",
   "symbols/UseProgramMain/description": "Indique s’il faut générer une classe Programme explicite et une méthode Main au lieu d’instructions de niveau supérieur.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Restaurez les packages NuGet requis par ce projet.",
   "postActions/restore/manualInstructions/default/text": "Exécuter « dotnet restore »"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.it.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.it.json
index 15792378214e..18be8dbf2fa2 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.it.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.it.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Se specificato, ignora il ripristino automatico del progetto durante la creazione.",
   "symbols/UseProgramMain/displayName": "Non usare_istruzioni di primo livello",
   "symbols/UseProgramMain/description": "Indica se generare una classe Program esplicita e un metodo Main anziché istruzioni di primo livello.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Ripristina i pacchetti NuGet richiesti da questo progetto.",
   "postActions/restore/manualInstructions/default/text": "Esegui 'dotnet restore'"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ja.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ja.json
index 16fad5c66aa0..04549054ce8f 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ja.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ja.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "指定した場合、作成時にプロジェクトの自動復元がスキップされます。",
   "symbols/UseProgramMain/displayName": "最上位レベルのステートメントを使用しない(_T)",
   "symbols/UseProgramMain/description": "最上位レベルのステートメントではなく、明示的な Program クラスと Main メソッドを生成するかどうか。",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "このプロジェクトに必要な NuGet パッケージを復元します。",
   "postActions/restore/manualInstructions/default/text": "'dotnet restore' を実行する"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ko.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ko.json
index 763695fd5a3e..795971474519 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ko.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ko.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "지정된 경우, 프로젝트 생성 시 자동 복원을 건너뜁니다.",
   "symbols/UseProgramMain/displayName": "최상위 문 사용 안 함(_T)",
   "symbols/UseProgramMain/description": "최상위 문 대신 명시적 Program 클래스 및 Main 메서드를 생성할지 여부입니다.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "이 프로젝트에 필요한 NuGet 패키지를 복원합니다.",
   "postActions/restore/manualInstructions/default/text": "'dotnet restore' 실행"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pl.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pl.json
index f85ea12cb58c..9d140822a380 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pl.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pl.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Jeśli ta opcja jest określona, pomija automatyczne przywracanie projektu podczas tworzenia.",
   "symbols/UseProgramMain/displayName": "Nie używaj ins_trukcji najwyższego poziomu",
   "symbols/UseProgramMain/description": "Określa, czy wygenerować jawną klasę Program i metodę Main zamiast instrukcji najwyższego poziomu.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Przywróć pakiety NuGet wymagane przez ten projekt.",
   "postActions/restore/manualInstructions/default/text": "Uruchom polecenie \"dotnet restore\""
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pt-BR.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pt-BR.json
index d56c2f98339b..387de16a6714 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pt-BR.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.pt-BR.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Se especificado, ignora a restauração automática do projeto sendo criado.",
   "symbols/UseProgramMain/displayName": "Não use ins_truções de nível superior",
   "symbols/UseProgramMain/description": "Se deve gerar uma classe de Programa explícita e um método principal em vez de instruções de nível superior.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Restaure os pacotes NuGet exigidos por este projeto.",
   "postActions/restore/manualInstructions/default/text": "Executa 'dotnet restore'"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ru.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ru.json
index b1303ffe207e..34073d1f5999 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ru.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.ru.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Если установлено, автоматическое восстановление проекта при создании пропускается.",
   "symbols/UseProgramMain/displayName": "Не использовать _операторы верхнего уровня",
   "symbols/UseProgramMain/description": "Следует ли создавать явный класс Program и метод Main вместо операторов верхнего уровня.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Восстановление пакетов NuGet, необходимых для этого проекта.",
   "postActions/restore/manualInstructions/default/text": "Выполнить команду \"dotnet restore\""
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.tr.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.tr.json
index 008a53a65f0f..c2b211a3eac5 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.tr.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.tr.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "Belirtilirse, oluşturma sırasında projenin otomatik geri yüklenmesini atlar.",
   "symbols/UseProgramMain/displayName": "_Üst düzey deyimler kullanmayın",
   "symbols/UseProgramMain/description": "Üst düzey deyimler yerine açık bir Program sınıfı ve Ana yöntem oluşturup oluşturulmayacağını belirtir.",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "Bu projenin gerektirdiği NuGet paketlerini geri yükleyin.",
   "postActions/restore/manualInstructions/default/text": "'dotnet restore' çalıştır"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hans.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hans.json
index 2247dc6d4b36..cedb5e3c71aa 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hans.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hans.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "如果指定，则在创建时跳过项目的自动还原。",
   "symbols/UseProgramMain/displayName": "不使用顶级语句(_T)",
   "symbols/UseProgramMain/description": "是否生成显式程序类和主方法，而不是顶级语句。",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "还原此项目所需的 NuGet 包。",
   "postActions/restore/manualInstructions/default/text": "运行 \"dotnet restore\""
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hant.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hant.json
index 7691752108c9..19940e8d352a 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hant.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/localize/templatestrings.zh-Hant.json
@@ -10,6 +10,7 @@
   "symbols/skipRestore/description": "若指定，會在建立時跳過專案的自動還原。",
   "symbols/UseProgramMain/displayName": "不要使用最上層陳述式(_T)",
   "symbols/UseProgramMain/description": "是否要產生明確的 Program 類別和 Main 方法，而非最上層語句。",
+  "symbols/DisableOpenAPI/description": "Disable OpenAPI (Swagger) support",
   "postActions/restore/description": "還原此專案所需的 NuGet 套件。",
   "postActions/restore/manualInstructions/default/text": "執行 'dotnet restore'"
 }
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/template.json b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/template.json
index bbc12adc0cc1..26f2ea88e496 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/template.json
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/.template.config/template.json
@@ -9,7 +9,7 @@
   ],
   "name": "ASP.NET Core Web API (native AOT)",
   "generatorVersions": "[1.0.0.0-*)",
-  "description": "A project template for creating a RESTful Web API using ASP.NET Core minimal APIs published as native AOT.",
+  "description": "A project template for creating a RESTful Web API using ASP.NET Core minimal APIs published as native AOT, with optional support for OpenAPI.",
   "groupIdentity": "Microsoft.Web.WebApiAot",
   "precedence": "10000",
   "identity": "Microsoft.Web.WebApiAot.CSharp.10.0",
@@ -130,6 +130,16 @@
       "defaultValue": "false",
       "displayName": "Do not use _top-level statements",
       "description": "Whether to generate an explicit Program class and Main method instead of top-level statements."
+    },
+    "DisableOpenAPI": {
+      "type": "parameter",
+      "dataType": "bool",
+      "defaultValue": "false",
+      "description": "Disable OpenAPI (Swagger) support"
+    },
+    "EnableOpenAPI": {
+      "type": "computed",
+      "value": "(!DisableOpenAPI)"
     }
   },
   "primaryOutputs": [
@@ -152,4 +162,4 @@
       "continueOnError": true
     }
   ]
-}
+}
\ No newline at end of file
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.Main.cs b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.Main.cs
index ea2807072a37..5cbfe789b9ed 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.Main.cs
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.Main.cs
@@ -1,4 +1,5 @@
 using System.Text.Json.Serialization;
+using Microsoft.AspNetCore.Http.HttpResults;
 
 namespace Company.WebApplication1;
 
@@ -13,8 +14,20 @@ public static void Main(string[] args)
             options.SerializerOptions.TypeInfoResolverChain.Insert(0, AppJsonSerializerContext.Default);
         });
 
+#if (EnableOpenAPI)
+        // Learn more about configuring OpenAPI at https://aka.ms/aspnet/openapi
+        builder.Services.AddOpenApi();
+#endif
+
         var app = builder.Build();
 
+#if (EnableOpenAPI)
+        if (app.Environment.IsDevelopment())
+        {
+            app.MapOpenApi();
+        }
+#endif
+
         var sampleTodos = new Todo[] {
             new(1, "Walk the dog"),
             new(2, "Do the dishes", DateOnly.FromDateTime(DateTime.Now)),
@@ -24,11 +37,23 @@ public static void Main(string[] args)
         };
 
         var todosApi = app.MapGroup("/todos");
+#if (EnableOpenAPI)
+        todosApi.MapGet("/", () => sampleTodos)
+                .WithName("GetTodos");
+
+        todosApi.MapGet("/{id}", Results<Ok<Todo>, NotFound> (int id) =>
+            sampleTodos.FirstOrDefault(a => a.Id == id) is { } todo
+                ? TypedResults.Ok(todo)
+                : TypedResults.NotFound())
+            .WithName("GetTodoById");
+#else
         todosApi.MapGet("/", () => sampleTodos);
-        todosApi.MapGet("/{id}", (int id) =>
+
+        todosApi.MapGet("/{id}", Results<Ok<Todo>, NotFound> (int id) =>
             sampleTodos.FirstOrDefault(a => a.Id == id) is { } todo
-                ? Results.Ok(todo)
-                : Results.NotFound());
+                ? TypedResults.Ok(todo)
+                : TypedResults.NotFound());
+#endif
 
         app.Run();
     }
diff --git a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.cs b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.cs
index d3b48c954001..819db8fb6a3a 100644
--- a/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.cs
+++ b/src/ProjectTemplates/Web.ProjectTemplates/content/WebApiAot-CSharp/Program.cs
@@ -1,4 +1,5 @@
 using System.Text.Json.Serialization;
+using Microsoft.AspNetCore.Http.HttpResults;
 
 var builder = WebApplication.CreateSlimBuilder(args);
 
@@ -7,8 +8,20 @@
     options.SerializerOptions.TypeInfoResolverChain.Insert(0, AppJsonSerializerContext.Default);
 });
 
+#if (EnableOpenAPI)
+// Learn more about configuring OpenAPI at https://aka.ms/aspnet/openapi
+builder.Services.AddOpenApi();
+#endif
+
 var app = builder.Build();
 
+#if (EnableOpenAPI)
+if (app.Environment.IsDevelopment())
+{
+    app.MapOpenApi();
+}
+#endif
+
 var sampleTodos = new Todo[] {
     new(1, "Walk the dog"),
     new(2, "Do the dishes", DateOnly.FromDateTime(DateTime.Now)),
@@ -18,11 +31,23 @@
 };
 
 var todosApi = app.MapGroup("/todos");
+#if (EnableOpenAPI)
+todosApi.MapGet("/", () => sampleTodos)
+        .WithName("GetTodos");
+
+todosApi.MapGet("/{id}", Results<Ok<Todo>, NotFound> (int id) =>
+    sampleTodos.FirstOrDefault(a => a.Id == id) is { } todo
+        ? TypedResults.Ok(todo)
+        : TypedResults.NotFound())
+    .WithName("GetTodoById");
+#else
 todosApi.MapGet("/", () => sampleTodos);
-todosApi.MapGet("/{id}", (int id) =>
+
+todosApi.MapGet("/{id}", Results<Ok<Todo>, NotFound> (int id) =>
     sampleTodos.FirstOrDefault(a => a.Id == id) is { } todo
-        ? Results.Ok(todo)
-        : Results.NotFound());
+        ? TypedResults.Ok(todo)
+        : TypedResults.NotFound());
+#endif
 
 app.Run();
 
diff --git a/src/ProjectTemplates/test/Templates.Tests/WebApiNativeAotTemplateTest.cs b/src/ProjectTemplates/test/Templates.Tests/WebApiNativeAotTemplateTest.cs
index 71c113aa7105..d1d6547c8484 100644
--- a/src/ProjectTemplates/test/Templates.Tests/WebApiNativeAotTemplateTest.cs
+++ b/src/ProjectTemplates/test/Templates.Tests/WebApiNativeAotTemplateTest.cs
@@ -34,17 +34,60 @@ public ITestOutputHelper Output
     [SkipOnHelix("https://github.com/dotnet/aspnetcore/issues/47478", Queues = HelixConstants.NativeAotNotSupportedHelixQueues)]
     public async Task WebApiNativeAotTemplateCSharp()
     {
-        await WebApiNativeAotTemplateCore(languageOverride: null);
+        await WebApiNativeAotTemplateCore(
+            languageOverride: null,
+            additionalEndpointsThatShould200OkForBuiltProjects: new[] { "/openapi/v1.json" });
     }
 
     [ConditionalFact]
     [SkipOnHelix("https://github.com/dotnet/aspnetcore/issues/47478", Queues = HelixConstants.NativeAotNotSupportedHelixQueues)]
     public async Task WebApiNativeAotTemplateProgramMainCSharp()
     {
-        await WebApiNativeAotTemplateCore(languageOverride: null, args: new[] { ArgConstants.UseProgramMain });
+        await WebApiNativeAotTemplateCore(
+            languageOverride: null,
+            args: new[] { ArgConstants.UseProgramMain },
+            additionalEndpointsThatShould200OkForBuiltProjects: new[] { "/openapi/v1.json" });
     }
 
-    private async Task WebApiNativeAotTemplateCore(string languageOverride, string[] args = null)
+    [ConditionalTheory]
+    [InlineData(false)]
+    [InlineData(true)]
+    [SkipOnHelix("https://github.com/dotnet/aspnetcore/issues/47478", Queues = HelixConstants.NativeAotNotSupportedHelixQueues)]
+    public async Task WebApiNativeAotTemplateCSharp_OpenApiDisabledInProductionEnvironment(bool useProgramMain)
+    {
+        var args = useProgramMain
+            ? new[] { ArgConstants.UseProgramMain }
+            : new string[] { };
+
+        await WebApiNativeAotTemplateCore(
+            languageOverride: null,
+            args: args,
+            additionalEndpointsThatShould404NotFoundForPublishedProjects: new[] { "/openapi/v1.json" });
+    }
+
+    [ConditionalTheory]
+    [InlineData(false)]
+    [InlineData(true)]
+    [SkipOnHelix("https://github.com/dotnet/aspnetcore/issues/47478", Queues = HelixConstants.NativeAotNotSupportedHelixQueues)]
+    public async Task WebApiNativeAotTemplateCSharp_WithoutOpenAPI(bool useProgramMain)
+    {
+        var args = useProgramMain
+            ? new[] { ArgConstants.UseProgramMain, ArgConstants.NoOpenApi }
+            : new[] { ArgConstants.NoOpenApi };
+
+        await WebApiNativeAotTemplateCore(
+            languageOverride: null,
+            args: args,
+            additionalEndpointsThatShould404NotFoundForBuiltProjects: new[] { "/openapi/v1.json" });
+    }
+
+    private async Task WebApiNativeAotTemplateCore(
+        string languageOverride,
+        string[] args = null,
+        string[] additionalEndpointsThatShould200OkForBuiltProjects = null,
+        string[] additionalEndpointsThatShould200OkForPublishedProjects = null,
+        string[] additionalEndpointsThatShould404NotFoundForBuiltProjects = null,
+        string[] additionalEndpointsThatShould404NotFoundForPublishedProjects = null)
     {
         var project = await ProjectFactory.CreateProject(Output);
         project.SetCurrentRuntimeIdentifier();
@@ -77,7 +120,7 @@ private async Task WebApiNativeAotTemplateCore(string languageOverride, string[]
             Assert.False(
                aspNetProcess.Process.HasExited,
                ErrorMessages.GetFailedProcessMessageOrEmpty("Run built project", project, aspNetProcess.Process));
-            await AssertEndpoints(aspNetProcess);
+            await AssertEndpoints(aspNetProcess, additionalEndpointsThatShould200OkForBuiltProjects, additionalEndpointsThatShould404NotFoundForBuiltProjects);
         }
 
         using (var aspNetProcess = project.StartPublishedProjectAsync(noHttps: true, usePublishedAppHost: true))
@@ -86,15 +129,31 @@ private async Task WebApiNativeAotTemplateCore(string languageOverride, string[]
                 aspNetProcess.Process.HasExited,
                 ErrorMessages.GetFailedProcessMessageOrEmpty("Run published project", project, aspNetProcess.Process));
 
-            await AssertEndpoints(aspNetProcess);
+            await AssertEndpoints(aspNetProcess, additionalEndpointsThatShould200OkForPublishedProjects, additionalEndpointsThatShould404NotFoundForPublishedProjects);
         }
     }
 
-    private async Task AssertEndpoints(AspNetProcess aspNetProcess)
+    private async Task AssertEndpoints(AspNetProcess aspNetProcess, string[] additionalEndpointsThatShould200Ok = null, string[] additionalEndpointsThatShould404NotFound = null)
     {
         await aspNetProcess.AssertOk("/todos");
         await aspNetProcess.AssertOk("/todos/1");
         await aspNetProcess.AssertNotFound("/todos/100");
         await aspNetProcess.AssertNotFound("/");
+
+        if (additionalEndpointsThatShould200Ok is not null)
+        {
+            foreach (var endpoint in additionalEndpointsThatShould200Ok)
+            {
+                await aspNetProcess.AssertOk(endpoint);
+            }
+        }
+
+        if (additionalEndpointsThatShould404NotFound is not null)
+        {
+            foreach (var endpoint in additionalEndpointsThatShould404NotFound)
+            {
+                await aspNetProcess.AssertNotFound(endpoint);
+            }
+        }
     }
 }