diff --git a/src/Microsoft.AspNetCore.Mvc.Core/Formatters/InputFormatter.cs b/src/Microsoft.AspNetCore.Mvc.Core/Formatters/InputFormatter.cs
index 8b9c00115f..c6fe0e94a1 100644
--- a/src/Microsoft.AspNetCore.Mvc.Core/Formatters/InputFormatter.cs
+++ b/src/Microsoft.AspNetCore.Mvc.Core/Formatters/InputFormatter.cs
@@ -6,6 +6,7 @@ using System.Collections.Generic;
 using System.Reflection;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Mvc.ApiExplorer;
+using Microsoft.AspNetCore.Mvc.Core;
 
 namespace Microsoft.AspNetCore.Mvc.Formatters
 {
@@ -43,6 +44,15 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
         /// <inheritdoc />
         public virtual bool CanRead(InputFormatterContext context)
         {
+            if (SupportedMediaTypes.Count == 0)
+            {
+                var message = Resources.FormatFormatter_NoMediaTypes(
+                    GetType().FullName,
+                    nameof(SupportedMediaTypes));
+
+                throw new InvalidOperationException(message);
+            }
+
             if (!CanReadType(context.ModelType))
             {
                 return false;
@@ -111,6 +121,15 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
         /// <inheritdoc />
         public virtual IReadOnlyList<string> GetSupportedContentTypes(string contentType, Type objectType)
         {
+            if (SupportedMediaTypes.Count == 0)
+            {
+                var message = Resources.FormatFormatter_NoMediaTypes(
+                    GetType().FullName,
+                    nameof(SupportedMediaTypes));
+
+                throw new InvalidOperationException(message);
+            }
+
             if (!CanReadType(objectType))
             {
                 return null;
@@ -119,7 +138,7 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             if (contentType == null)
             {
                 // If contentType is null, then any type we support is valid.
-                return SupportedMediaTypes.Count > 0 ? SupportedMediaTypes : null;
+                return SupportedMediaTypes;
             }
             else
             {
diff --git a/src/Microsoft.AspNetCore.Mvc.Core/Formatters/OutputFormatter.cs b/src/Microsoft.AspNetCore.Mvc.Core/Formatters/OutputFormatter.cs
index 314fadbfe9..9ba3d68b3e 100644
--- a/src/Microsoft.AspNetCore.Mvc.Core/Formatters/OutputFormatter.cs
+++ b/src/Microsoft.AspNetCore.Mvc.Core/Formatters/OutputFormatter.cs
@@ -5,6 +5,7 @@ using System;
 using System.Collections.Generic;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Mvc.ApiExplorer;
+using Microsoft.AspNetCore.Mvc.Core;
 using Microsoft.Extensions.Primitives;
 
 namespace Microsoft.AspNetCore.Mvc.Formatters
@@ -14,19 +15,11 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
     /// </summary>
     public abstract class OutputFormatter : IOutputFormatter, IApiResponseFormatMetadataProvider
     {
-        /// <summary>
-        /// Initializes a new instance of the <see cref="OutputFormatter"/> class.
-        /// </summary>
-        protected OutputFormatter()
-        {
-            SupportedMediaTypes = new MediaTypeCollection();
-        }
-
         /// <summary>
         /// Gets the mutable collection of media type elements supported by
         /// this <see cref="OutputFormatter"/>.
         /// </summary>
-        public MediaTypeCollection SupportedMediaTypes { get; }
+        public MediaTypeCollection SupportedMediaTypes { get; } = new MediaTypeCollection();
 
         /// <summary>
         /// Returns a value indicating whether or not the given type can be written by this serializer.
@@ -43,6 +36,15 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             string contentType,
             Type objectType)
         {
+            if (SupportedMediaTypes.Count == 0)
+            {
+                var message = Resources.FormatFormatter_NoMediaTypes(
+                    GetType().FullName,
+                    nameof(SupportedMediaTypes));
+
+                throw new InvalidOperationException(message);
+            }
+
             if (!CanWriteType(objectType))
             {
                 return null;
@@ -51,7 +53,7 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             if (contentType == null)
             {
                 // If contentType is null, then any type we support is valid.
-                return SupportedMediaTypes.Count > 0 ? SupportedMediaTypes : null;
+                return SupportedMediaTypes;
             }
             else
             {
@@ -87,6 +89,15 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
                 throw new ArgumentNullException(nameof(context));
             }
 
+            if (SupportedMediaTypes.Count == 0)
+            {
+                var message = Resources.FormatFormatter_NoMediaTypes(
+                    GetType().FullName,
+                    nameof(SupportedMediaTypes));
+
+                throw new InvalidOperationException(message);
+            }
+
             if (!CanWriteType(context.ObjectType))
             {
                 return false;
@@ -96,15 +107,8 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             {
                 // If the desired content type is set to null, then the current formatter can write anything
                 // it wants.
-                if (SupportedMediaTypes.Count > 0)
-                {
-                    context.ContentType = new StringSegment(SupportedMediaTypes[0]);
-                    return true;
-                }
-                else
-                {
-                    return false;
-                }
+                context.ContentType = new StringSegment(SupportedMediaTypes[0]);
+                return true;
             }
             else
             {
@@ -160,4 +164,4 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
         /// <returns>A task which can write the response body.</returns>
         public abstract Task WriteResponseBodyAsync(OutputFormatterWriteContext context);
     }
-}
\ No newline at end of file
+}
diff --git a/src/Microsoft.AspNetCore.Mvc.Core/Properties/Resources.Designer.cs b/src/Microsoft.AspNetCore.Mvc.Core/Properties/Resources.Designer.cs
index db8b79a02b..55a474f187 100644
--- a/src/Microsoft.AspNetCore.Mvc.Core/Properties/Resources.Designer.cs
+++ b/src/Microsoft.AspNetCore.Mvc.Core/Properties/Resources.Designer.cs
@@ -1146,6 +1146,22 @@ namespace Microsoft.AspNetCore.Mvc.Core
             return string.Format(CultureInfo.CurrentCulture, GetString("TextOutpurFormatter_WriteResponseBodyAsynNotSupported"), p0, p1, p2);
         }
 
+        /// <summary>
+        /// No media types found in '{0}.{1}'. Add at least one media type to the list of supported media types.
+        /// </summary>
+        internal static string Formatter_NoMediaTypes
+        {
+            get { return GetString("Formatter_NoMediaTypes"); }
+        }
+
+        /// <summary>
+        /// No media types found in '{0}.{1}'. Add at least one media type to the list of supported media types.
+        /// </summary>
+        internal static string FormatFormatter_NoMediaTypes(object p0, object p1)
+        {
+            return string.Format(CultureInfo.CurrentCulture, GetString("Formatter_NoMediaTypes"), p0, p1);
+        }
+
         private static string GetString(string name, params string[] formatterNames)
         {
             var value = _resourceManager.GetString(name);
diff --git a/src/Microsoft.AspNetCore.Mvc.Core/Resources.resx b/src/Microsoft.AspNetCore.Mvc.Core/Resources.resx
index 84d1befc53..04dc1391b1 100644
--- a/src/Microsoft.AspNetCore.Mvc.Core/Resources.resx
+++ b/src/Microsoft.AspNetCore.Mvc.Core/Resources.resx
@@ -1,17 +1,17 @@
 <?xml version="1.0" encoding="utf-8"?>
 <root>
-  <!-- 
-    Microsoft ResX Schema 
-    
+  <!--
+    Microsoft ResX Schema
+
     Version 2.0
-    
-    The primary goals of this format is to allow a simple XML format 
-    that is mostly human readable. The generation and parsing of the 
-    various data types are done through the TypeConverter classes 
+
+    The primary goals of this format is to allow a simple XML format
+    that is mostly human readable. The generation and parsing of the
+    various data types are done through the TypeConverter classes
     associated with the data types.
-    
+
     Example:
-    
+
     ... ado.net/XML headers & schema ...
     <resheader name="resmimetype">text/microsoft-resx</resheader>
     <resheader name="version">2.0</resheader>
@@ -26,36 +26,36 @@
         <value>[base64 mime encoded string representing a byte array form of the .NET Framework object]</value>
         <comment>This is a comment</comment>
     </data>
-                
-    There are any number of "resheader" rows that contain simple 
+
+    There are any number of "resheader" rows that contain simple
     name/value pairs.
-    
-    Each data row contains a name, and value. The row also contains a 
-    type or mimetype. Type corresponds to a .NET class that support 
-    text/value conversion through the TypeConverter architecture. 
-    Classes that don't support this are serialized and stored with the 
+
+    Each data row contains a name, and value. The row also contains a
+    type or mimetype. Type corresponds to a .NET class that support
+    text/value conversion through the TypeConverter architecture.
+    Classes that don't support this are serialized and stored with the
     mimetype set.
-    
-    The mimetype is used for serialized objects, and tells the 
-    ResXResourceReader how to depersist the object. This is currently not 
+
+    The mimetype is used for serialized objects, and tells the
+    ResXResourceReader how to depersist the object. This is currently not
     extensible. For a given mimetype the value must be set accordingly:
-    
-    Note - application/x-microsoft.net.object.binary.base64 is the format 
-    that the ResXResourceWriter will generate, however the reader can 
+
+    Note - application/x-microsoft.net.object.binary.base64 is the format
+    that the ResXResourceWriter will generate, however the reader can
     read any of the formats listed below.
-    
+
     mimetype: application/x-microsoft.net.object.binary.base64
-    value   : The object must be serialized with 
+    value   : The object must be serialized with
             : System.Runtime.Serialization.Formatters.Binary.BinaryFormatter
             : and then encoded with base64 encoding.
-    
+
     mimetype: application/x-microsoft.net.object.soap.base64
-    value   : The object must be serialized with 
+    value   : The object must be serialized with
             : System.Runtime.Serialization.Formatters.Soap.SoapFormatter
             : and then encoded with base64 encoding.
 
     mimetype: application/x-microsoft.net.object.bytearray.base64
-    value   : The object must be serialized into a byte array 
+    value   : The object must be serialized into a byte array
             : using a System.ComponentModel.TypeConverter
             : and then encoded with base64 encoding.
     -->
@@ -340,4 +340,7 @@
   <data name="TextOutpurFormatter_WriteResponseBodyAsynNotSupported" xml:space="preserve">
     <value>'{0}' is not supported by '{1}'. Use '{2}' instead.</value>
   </data>
+  <data name="Formatter_NoMediaTypes" xml:space="preserve">
+    <value>No media types found in '{0}.{1}'. Add at least one media type to the list of supported media types.</value>
+  </data>
 </root>
\ No newline at end of file
diff --git a/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/InputFormatterTest.cs b/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/InputFormatterTest.cs
index 6ddb2d3838..eae5c6eecd 100644
--- a/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/InputFormatterTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/InputFormatterTest.cs
@@ -3,6 +3,7 @@
 
 using System;
 using System.Collections.Generic;
+using System.IO;
 using System.Linq;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Http.Internal;
@@ -382,6 +383,41 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             Assert.Collection(results, c => Assert.Equal("text/xml", c));
         }
 
+        [Fact]
+        public void CanRead_ThrowsInvalidOperationException_IfMediaTypesListIsEmpty()
+        {
+            // Arrange
+            var formatter = new BadConfigurationFormatter();
+            var context = new InputFormatterContext(
+                new DefaultHttpContext(),
+                "",
+                new ModelStateDictionary(),
+                new EmptyModelMetadataProvider().GetMetadataForType(typeof(object)),
+                (s, e) => new StreamReader(s, e));
+
+            // Act & Assert
+            Assert.Throws<InvalidOperationException>(() => formatter.CanRead(context));
+        }
+
+        [Fact]
+        public void GetSupportedContentTypes_ThrowsInvalidOperationException_IfMediaTypesListIsEmpty()
+        {
+            // Arrange
+            var formatter = new BadConfigurationFormatter();
+
+            // Act & Assert
+            Assert.Throws<InvalidOperationException>(
+                () => formatter.GetSupportedContentTypes("application/json", typeof(object)));
+        }
+
+        private class BadConfigurationFormatter : InputFormatter
+        {
+            public override Task<InputFormatterResult> ReadRequestBodyAsync(InputFormatterContext context)
+            {
+                throw new NotImplementedException();
+            }
+        }
+
         private class TestFormatter : InputFormatter
         {
             public IList<Type> SupportedTypes { get; } = new List<Type>();
diff --git a/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/OutputFormatterTests.cs b/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/OutputFormatterTests.cs
index 6476947fd5..20407b07fe 100644
--- a/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/OutputFormatterTests.cs
+++ b/test/Microsoft.AspNetCore.Mvc.Core.Test/Formatters/OutputFormatterTests.cs
@@ -3,6 +3,7 @@
 
 using System;
 using System.Collections.Generic;
+using System.IO;
 using System.Text;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Http;
@@ -138,24 +139,6 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             Assert.Null(contentTypes);
         }
 
-        [Fact]
-        public void GetSupportedContentTypes_ReturnsAllContentTypes_ReturnsNullWithNoSupportedContentTypes()
-        {
-            // Arrange
-            var formatter = new TestOutputFormatter();
-
-            // Intentionally empty
-            formatter.SupportedMediaTypes.Clear();
-
-            // Act
-            var contentTypes = formatter.GetSupportedContentTypes(
-                contentType: null,
-                objectType: typeof(int));
-
-            // Assert
-            Assert.Null(contentTypes);
-        }
-
         private class TypeSpecificFormatter : OutputFormatter
         {
             public List<Type> SupportedTypes { get; } = new List<Type>();
@@ -171,6 +154,35 @@ namespace Microsoft.AspNetCore.Mvc.Formatters
             }
         }
 
+        [Fact]
+        public void CanWrite_ThrowsInvalidOperationException_IfMediaTypesListIsEmpty()
+        {
+            // Arrange
+            var formatter = new TestOutputFormatter();
+            formatter.SupportedMediaTypes.Clear();
+
+            var context = new OutputFormatterWriteContext(
+                new DefaultHttpContext(),
+                (s, e) => new StreamWriter(s, e),
+                typeof(object),
+                new object());
+
+            // Act & Assert
+            Assert.Throws<InvalidOperationException>(() => formatter.CanWriteResult(context));
+        }
+
+        [Fact]
+        public void GetSupportedContentTypes_ThrowsInvalidOperationException_IfMediaTypesListIsEmpty()
+        {
+            // Arrange
+            var formatter = new TestOutputFormatter();
+            formatter.SupportedMediaTypes.Clear();
+
+            // Act & Assert
+            Assert.Throws<InvalidOperationException>(
+                () => formatter.GetSupportedContentTypes("application/json", typeof(object)));
+        }
+
         private class TestOutputFormatter : OutputFormatter
         {
             public TestOutputFormatter()