diff --git a/src/OpenApi/sample/Controllers/TestController.cs b/src/OpenApi/sample/Controllers/TestController.cs
index c3c011c61385..43a1e22250f9 100644
--- a/src/OpenApi/sample/Controllers/TestController.cs
+++ b/src/OpenApi/sample/Controllers/TestController.cs
@@ -60,10 +60,10 @@ public class HttpFoo() : HttpMethodAttribute(["FOO"]);
 
     public class RouteParamsContainer
     {
-        [FromRoute]
+        [FromRoute(Name = "id")]
         public int Id { get; set; }
 
-        [FromRoute]
+        [FromRoute(Name = "name")]
         [MinLength(5)]
         [UnconditionalSuppressMessage("Trimming", "IL2026:RequiresUnreferencedCode", Justification = "MinLengthAttribute works without reflection on string properties.")]
         public string? Name { get; set; }
diff --git a/src/OpenApi/src/Extensions/ApiDescriptionExtensions.cs b/src/OpenApi/src/Extensions/ApiDescriptionExtensions.cs
index 20c19c02a258..40757002dc2d 100644
--- a/src/OpenApi/src/Extensions/ApiDescriptionExtensions.cs
+++ b/src/OpenApi/src/Extensions/ApiDescriptionExtensions.cs
@@ -28,7 +28,7 @@ internal static class ApiDescriptionExtensions
             "HEAD" => HttpMethod.Head,
             "OPTIONS" => HttpMethod.Options,
             "TRACE" => HttpMethod.Trace,
-            "QUERY" => HttpMethod.Query,
+            "QUERY" => null, // OpenAPI as of 3.1 does not yet support HTTP QUERY
             _ => null,
         };
 
diff --git a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/OpenApiDocumentIntegrationTests.cs b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/OpenApiDocumentIntegrationTests.cs
index 1ce73bd3e57c..e9b5441087a2 100644
--- a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/OpenApiDocumentIntegrationTests.cs
+++ b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/OpenApiDocumentIntegrationTests.cs
@@ -36,10 +36,7 @@ public static TheoryData<string, OpenApiSpecVersion> OpenApiDocuments()
     [MemberData(nameof(OpenApiDocuments))]
     public async Task VerifyOpenApiDocument(string documentName, OpenApiSpecVersion version)
     {
-        var documentService = fixture.Services.GetRequiredKeyedService<OpenApiDocumentService>(documentName);
-        var scopedServiceProvider = fixture.Services.CreateScope();
-        var document = await documentService.GetOpenApiDocumentAsync(scopedServiceProvider.ServiceProvider);
-        var json = await document.SerializeAsJsonAsync(version);
+        var json = await GetOpenApiDocument(documentName, version);
         var baseSnapshotsDirectory = SkipOnHelixAttribute.OnHelix()
             ? Path.Combine(Environment.GetEnvironmentVariable("HELIX_WORKITEM_ROOT"), "Integration", "snapshots")
             : "snapshots";
@@ -48,4 +45,32 @@ await Verify(json)
             .UseDirectory(outputDirectory)
             .UseParameters(documentName);
     }
+
+    [Theory]
+    [MemberData(nameof(OpenApiDocuments))]
+    public async Task OpenApiDocumentIsValid(string documentName, OpenApiSpecVersion version)
+    {
+        var json = await GetOpenApiDocument(documentName, version);
+
+        var actual = OpenApiDocument.Parse(json, format: "json");
+
+        Assert.NotNull(actual);
+        Assert.NotNull(actual.Document);
+        Assert.NotNull(actual.Diagnostic);
+        Assert.NotNull(actual.Diagnostic.Errors);
+        Assert.Empty(actual.Diagnostic.Errors);
+
+        var ruleSet = ValidationRuleSet.GetDefaultRuleSet();
+
+        var errors = actual.Document.Validate(ruleSet);
+        Assert.Empty(errors);
+    }
+
+    private async Task<string> GetOpenApiDocument(string documentName, OpenApiSpecVersion version)
+    {
+        var documentService = fixture.Services.GetRequiredKeyedService<OpenApiDocumentService>(documentName);
+        var scopedServiceProvider = fixture.Services.CreateScope();
+        var document = await documentService.GetOpenApiDocumentAsync(scopedServiceProvider.ServiceProvider);
+        return await document.SerializeAsJsonAsync(version);
+    }
 }
diff --git a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_0/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_0/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
index 5f9f4d1dd9e6..07aaa0b07c41 100644
--- a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_0/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
+++ b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_0/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
@@ -12,7 +12,7 @@
         ],
         "parameters": [
           {
-            "name": "Id",
+            "name": "id",
             "in": "path",
             "required": true,
             "schema": {
@@ -21,7 +21,7 @@
             }
           },
           {
-            "name": "Name",
+            "name": "name",
             "in": "path",
             "required": true,
             "schema": {
@@ -124,35 +124,6 @@
           }
         }
       }
-    },
-    "/query": {
-      "query": {
-        "tags": [
-          "Test"
-        ],
-        "responses": {
-          "200": {
-            "description": "OK",
-            "content": {
-              "text/plain": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "application/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "text/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              }
-            }
-          }
-        }
-      }
     }
   },
   "components": {
diff --git a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_1/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_1/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
index f41a4ddb6a43..54815495aa78 100644
--- a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_1/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
+++ b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApi3_1/OpenApiDocumentIntegrationTests.VerifyOpenApiDocument_documentName=controllers.verified.txt
@@ -12,7 +12,7 @@
         ],
         "parameters": [
           {
-            "name": "Id",
+            "name": "id",
             "in": "path",
             "required": true,
             "schema": {
@@ -21,7 +21,7 @@
             }
           },
           {
-            "name": "Name",
+            "name": "name",
             "in": "path",
             "required": true,
             "schema": {
@@ -124,35 +124,6 @@
           }
         }
       }
-    },
-    "/query": {
-      "query": {
-        "tags": [
-          "Test"
-        ],
-        "responses": {
-          "200": {
-            "description": "OK",
-            "content": {
-              "text/plain": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "application/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "text/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              }
-            }
-          }
-        }
-      }
     }
   },
   "components": {
diff --git a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApiDocumentLocalizationTests.VerifyOpenApiDocumentIsInvariant.verified.txt b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApiDocumentLocalizationTests.VerifyOpenApiDocumentIsInvariant.verified.txt
index f7870bc2fe95..4c8502f366b3 100644
--- a/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApiDocumentLocalizationTests.VerifyOpenApiDocumentIsInvariant.verified.txt
+++ b/src/OpenApi/test/Microsoft.AspNetCore.OpenApi.Tests/Integration/snapshots/OpenApiDocumentLocalizationTests.VerifyOpenApiDocumentIsInvariant.verified.txt
@@ -1165,7 +1165,7 @@
         ],
         "parameters": [
           {
-            "name": "Id",
+            "name": "id",
             "in": "path",
             "required": true,
             "schema": {
@@ -1174,7 +1174,7 @@
             }
           },
           {
-            "name": "Name",
+            "name": "name",
             "in": "path",
             "required": true,
             "schema": {
@@ -1277,35 +1277,6 @@
           }
         }
       }
-    },
-    "/query": {
-      "query": {
-        "tags": [
-          "Test"
-        ],
-        "responses": {
-          "200": {
-            "description": "OK",
-            "content": {
-              "text/plain": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "application/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              },
-              "text/json": {
-                "schema": {
-                  "$ref": "#/components/schemas/CurrentWeather"
-                }
-              }
-            }
-          }
-        }
-      }
     }
   },
   "components": {