diff --git a/src/libraries/System.Text.Json/src/Resources/Strings.resx b/src/libraries/System.Text.Json/src/Resources/Strings.resx
index b67fc02b7a5a86..8b259b4fa14212 100644
--- a/src/libraries/System.Text.Json/src/Resources/Strings.resx
+++ b/src/libraries/System.Text.Json/src/Resources/Strings.resx
@@ -232,7 +232,7 @@
     <value>'{0}' is invalid within a JSON string. The string should be correctly escaped.</value>
   </data>
   <data name="UnsupportedEnumIdentifier" xml:space="preserve">
-    <value>Enum type '{0}' uses unsupported identifier '{1}'. It must not be null, empty, or containing leading or trailing whitespace. Flags enums must additionally not contain commas.</value>
+    <value>Enum type '{0}' uses unsupported identifier '{1}'. It must not be null nor contain leading or trailing whitespace. Flags enums must additionally not be empty nor contain commas.</value>
   </data>
   <data name="InvalidEndOfJsonNonPrimitive" xml:space="preserve">
     <value>'{0}' is an invalid token type for the end of the JSON payload. Expected either 'EndArray' or 'EndObject'.</value>
diff --git a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Converters/Value/EnumConverter.cs b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Converters/Value/EnumConverter.cs
index ebc89780decd41..0d2d7a70bb4aec 100644
--- a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Converters/Value/EnumConverter.cs
+++ b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Converters/Value/EnumConverter.cs
@@ -304,9 +304,26 @@ private bool TryParseNamedEnum(
         {
 #if NET
             Dictionary<string, EnumFieldInfo>.AlternateLookup<ReadOnlySpan<char>> lookup = _enumFieldInfoIndex.GetAlternateLookup<ReadOnlySpan<char>>();
-            ReadOnlySpan<char> rest = source;
 #else
             Dictionary<string, EnumFieldInfo> lookup = _enumFieldInfoIndex;
+#endif
+
+            if (!s_isFlagsEnum)
+            {
+                if (lookup.TryGetValue(source, out EnumFieldInfo? firstResult) &&
+                    firstResult.GetMatchingField(source) is EnumFieldInfo match)
+                {
+                    result = ConvertFromUInt64(match.Key);
+                    return true;
+                }
+
+                result = default;
+                return false;
+            }
+
+#if NET
+            ReadOnlySpan<char> rest = source;
+#else
             ReadOnlySpan<char> rest = source.AsSpan();
 #endif
             ulong key = 0;
@@ -572,11 +589,13 @@ private static string ResolveAndValidateJsonName(string name, JsonNamingPolicy?
                 name = namingPolicy.ConvertName(name);
             }
 
-            if (string.IsNullOrEmpty(name) || char.IsWhiteSpace(name[0]) || char.IsWhiteSpace(name[name.Length - 1]) ||
-                (s_isFlagsEnum && name.Contains(',')))
+            if (name is null ||
+                (name.Length > 0 && (char.IsWhiteSpace(name[0]) || char.IsWhiteSpace(name[name.Length - 1]))) ||
+                (s_isFlagsEnum && (name.Length == 0 || name.Contains(','))))
             {
-                // Reject null or empty strings or strings with leading or trailing whitespace.
-                // In the case of flags additionally reject strings containing commas.
+                // Reject null strings or strings with leading or trailing whitespace.
+                // In the case of flags additionally reject empty strings or strings containing commas,
+                // both of which would introduce ambiguity in flag value parsing and formatting.
                 ThrowHelper.ThrowInvalidOperationException_UnsupportedEnumIdentifier(typeof(T), name);
             }
 
diff --git a/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/EnumConverterTests.cs b/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/EnumConverterTests.cs
index ada90fab227649..12e6c557ceb66e 100644
--- a/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/EnumConverterTests.cs
+++ b/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/EnumConverterTests.cs
@@ -1259,6 +1259,7 @@ public enum EnumWithInvalidMemberName1
             Value
         }
 
+        [Flags]
         public enum EnumWithInvalidMemberName2
         {
             [JsonStringEnumMemberName("")]
@@ -1290,6 +1291,65 @@ public enum EnumWithInvalidMemberName6
             Value
         }
 
+        [Theory]
+        [InlineData(YesOrNoOrEmpty.Yes, "\"y\"")]
+        [InlineData(YesOrNoOrEmpty.No, "\"n\"")]
+        [InlineData(YesOrNoOrEmpty.Empty, "\"\"")]
+        public static void EnumWithEmptyStringMemberName_NonFlags_RoundtripsAsExpected(YesOrNoOrEmpty value, string expectedJson)
+        {
+            string json = JsonSerializer.Serialize(value, s_optionsWithStringEnumConverter);
+            Assert.Equal(expectedJson, json);
+            Assert.Equal(value, JsonSerializer.Deserialize<YesOrNoOrEmpty>(json, s_optionsWithStringEnumConverter));
+        }
+
+        [Theory]
+        [InlineData("\"y, , n\"")]
+        [InlineData("\",\"")]
+        [InlineData("\"y,n\"")]
+        public static void EnumWithEmptyStringMemberName_NonFlags_DoesNotParseCommaSeparatedValues(string json)
+        {
+            Assert.Throws<JsonException>(() => JsonSerializer.Deserialize<YesOrNoOrEmpty>(json, s_optionsWithStringEnumConverter));
+        }
+
+        public enum YesOrNoOrEmpty
+        {
+            [JsonStringEnumMemberName("y")]
+            Yes,
+
+            [JsonStringEnumMemberName("n")]
+            No,
+
+            [JsonStringEnumMemberName("")]
+            Empty,
+        }
+
+        [Fact]
+        public static void EnumWithEmptyStringMemberName_Flags_Throws()
+        {
+            string expectedExceptionMessage = $"Enum type '{nameof(YesOrNoOrEmptyFlags)}' uses unsupported identifier ''.";
+
+            InvalidOperationException ex = Assert.Throws<InvalidOperationException>(
+                () => JsonSerializer.Serialize(YesOrNoOrEmptyFlags.Yes, s_optionsWithStringEnumConverter));
+            Assert.Contains(expectedExceptionMessage, ex.Message);
+
+            ex = Assert.Throws<InvalidOperationException>(
+                () => JsonSerializer.Deserialize<YesOrNoOrEmptyFlags>("\"y\"", s_optionsWithStringEnumConverter));
+            Assert.Contains(expectedExceptionMessage, ex.Message);
+        }
+
+        [Flags]
+        public enum YesOrNoOrEmptyFlags
+        {
+            [JsonStringEnumMemberName("y")]
+            Yes = 1,
+
+            [JsonStringEnumMemberName("n")]
+            No = 2,
+
+            [JsonStringEnumMemberName("")]
+            Empty = 4,
+        }
+
         [Theory]
         [InlineData("\"cAmElCaSe\"", EnumWithVaryingNamingPolicies.camelCase, JsonKnownNamingPolicy.SnakeCaseUpper)]
         [InlineData("\"cAmElCaSe\"", EnumWithVaryingNamingPolicies.camelCase, JsonKnownNamingPolicy.SnakeCaseLower)]