diff --git a/src/Http/Http.Abstractions/src/Validation/ValidatableTypeInfo.cs b/src/Http/Http.Abstractions/src/Validation/ValidatableTypeInfo.cs
index 6bf3ff182d19..a20f0ec8a800 100644
--- a/src/Http/Http.Abstractions/src/Validation/ValidatableTypeInfo.cs
+++ b/src/Http/Http.Abstractions/src/Validation/ValidatableTypeInfo.cs
@@ -104,12 +104,20 @@ public virtual async Task ValidateAsync(object? value, ValidateContext context,
                 {
                     if (validationResult != ValidationResult.Success && validationResult.ErrorMessage is not null)
                     {
-                        var memberName = validationResult.MemberNames.First();
-                        var key = string.IsNullOrEmpty(originalPrefix) ?
-                            memberName :
-                            $"{originalPrefix}.{memberName}";
-
-                        context.AddOrExtendValidationError(key, validationResult.ErrorMessage);
+                        // Create a validation error for each member name that is provided
+                        foreach (var memberName in validationResult.MemberNames)
+                        {
+                            var key = string.IsNullOrEmpty(originalPrefix) ?
+                                memberName :
+                                $"{originalPrefix}.{memberName}";
+                            context.AddOrExtendValidationError(key, validationResult.ErrorMessage);
+                        }
+
+                        if (!validationResult.MemberNames.Any())
+                        {
+                            // If no member names are specified, then treat this as a top-level error
+                            context.AddOrExtendValidationError(string.Empty, validationResult.ErrorMessage);
+                        }
                     }
                 }
 
diff --git a/src/Http/Http.Abstractions/test/Validation/ValidatableTypeInfoTests.cs b/src/Http/Http.Abstractions/test/Validation/ValidatableTypeInfoTests.cs
index fe75387e8e22..2a4c82e704e5 100644
--- a/src/Http/Http.Abstractions/test/Validation/ValidatableTypeInfoTests.cs
+++ b/src/Http/Http.Abstractions/test/Validation/ValidatableTypeInfoTests.cs
@@ -495,6 +495,95 @@ public async Task Validate_RequiredOnPropertyShortCircuitsOtherValidations()
         Assert.Equal("The Password field is required.", error.Value.Single());
     }
 
+    [Fact]
+    public async Task Validate_IValidatableObject_WithZeroAndMultipleMemberNames_BehavesAsExpected()
+    {
+        var globalType = new TestValidatableTypeInfo(
+            typeof(GlobalErrorObject),
+            []); // no properties – nothing sets MemberName
+
+        var context = new ValidateContext
+        {
+            ValidationOptions = new TestValidationOptions(new Dictionary<Type, ValidatableTypeInfo>
+            {
+                { typeof(GlobalErrorObject), globalType }
+            })
+        };
+
+        var globalErrorInstance = new GlobalErrorObject { Data = -1 };
+        context.ValidationContext = new ValidationContext(globalErrorInstance);
+
+        await globalType.ValidateAsync(globalErrorInstance, context, default);
+
+        Assert.NotNull(context.ValidationErrors);
+        var globalError = Assert.Single(context.ValidationErrors);
+        Assert.Equal(string.Empty, globalError.Key);
+        Assert.Equal("Data must be positive.", globalError.Value.Single());
+
+        var multiType = new TestValidatableTypeInfo(
+            typeof(MultiMemberErrorObject),
+            [
+                CreatePropertyInfo(typeof(MultiMemberErrorObject), typeof(string), "FirstName", "FirstName", []),
+                CreatePropertyInfo(typeof(MultiMemberErrorObject), typeof(string), "LastName",  "LastName",  [])
+            ]);
+
+        context.ValidationErrors = [];
+        context.ValidationOptions = new TestValidationOptions(new Dictionary<Type, ValidatableTypeInfo>
+        {
+            { typeof(MultiMemberErrorObject), multiType }
+        });
+
+        var multiErrorInstance = new MultiMemberErrorObject { FirstName = "", LastName = "" };
+        context.ValidationContext = new ValidationContext(multiErrorInstance);
+
+        await multiType.ValidateAsync(multiErrorInstance, context, default);
+
+        Assert.NotNull(context.ValidationErrors);
+        Assert.Collection(context.ValidationErrors,
+            kvp =>
+            {
+                Assert.Equal("FirstName", kvp.Key);
+                Assert.Equal("FirstName and LastName are required.", kvp.Value.First());
+            },
+            kvp =>
+            {
+                Assert.Equal("LastName", kvp.Key);
+                Assert.Equal("FirstName and LastName are required.", kvp.Value.First());
+            });
+    }
+
+    // Returns no member names to validate https://github.com/dotnet/aspnetcore/issues/61739
+    private class GlobalErrorObject : IValidatableObject
+    {
+        public int Data { get; set; }
+
+        public IEnumerable<ValidationResult> Validate(ValidationContext validationContext)
+        {
+            if (Data <= 0)
+            {
+                yield return new ValidationResult("Data must be positive.");
+            }
+        }
+    }
+
+    // Returns multiple member names to validate https://github.com/dotnet/aspnetcore/issues/61739
+    private class MultiMemberErrorObject : IValidatableObject
+    {
+        public string? FirstName { get; set; }
+        public string? LastName { get; set; }
+
+        public IEnumerable<ValidationResult> Validate(ValidationContext validationContext)
+        {
+            if (string.IsNullOrEmpty(FirstName) || string.IsNullOrEmpty(LastName))
+            {
+                // MULTIPLE member names
+                yield return new ValidationResult(
+                    "FirstName and LastName are required.",
+                    [nameof(FirstName), nameof(LastName)]);
+            }
+        }
+    }
+
     private ValidatablePropertyInfo CreatePropertyInfo(
         Type containingType,
         Type propertyType,
@@ -534,7 +623,7 @@ public IEnumerable<ValidationResult> Validate(ValidationContext validationContex
         {
             if (Salary < 0)
             {
-                yield return new ValidationResult("Salary must be a positive value.", new[] { nameof(Salary) });
+                yield return new ValidationResult("Salary must be a positive value.", ["Salary"]);
             }
         }
     }