diff --git a/src/execution/__tests__/oneof-test.ts b/src/execution/__tests__/oneof-test.ts
index 0416cccd2d..85153c244a 100644
--- a/src/execution/__tests__/oneof-test.ts
+++ b/src/execution/__tests__/oneof-test.ts
@@ -83,7 +83,7 @@ describe('Execute: Handles OneOf Input Objects', () => {
           {
             locations: [{ column: 16, line: 2 }],
             message:
-              'Variable "$input" has invalid default value: OneOf Input Object "TestInputObject" must specify exactly one key.',
+              'Variable "$input" has invalid default value: Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           },
         ],
       });
@@ -148,7 +148,7 @@ describe('Execute: Handles OneOf Input Objects', () => {
         errors: [
           {
             message:
-              'Variable "$input" has invalid value: Field "a" for OneOf type "TestInputObject" must be non-null.',
+              'Variable "$input" has invalid value at .a: Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
             locations: [{ line: 2, column: 16 }],
           },
         ],
@@ -173,7 +173,7 @@ describe('Execute: Handles OneOf Input Objects', () => {
           {
             locations: [{ column: 16, line: 2 }],
             message:
-              'Variable "$input" has invalid value: Exactly one key must be specified for OneOf type "TestInputObject".',
+              'Variable "$input" has invalid value: Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           },
         ],
       });
@@ -197,7 +197,7 @@ describe('Execute: Handles OneOf Input Objects', () => {
           {
             locations: [{ column: 16, line: 2 }],
             message:
-              'Variable "$input" has invalid value: Exactly one key must be specified for OneOf type "TestInputObject".',
+              'Variable "$input" has invalid value: Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           },
         ],
       });
diff --git a/src/utilities/__tests__/validateInputValue-test.ts b/src/utilities/__tests__/validateInputValue-test.ts
index 6aaae7188a..82c6814b56 100644
--- a/src/utilities/__tests__/validateInputValue-test.ts
+++ b/src/utilities/__tests__/validateInputValue-test.ts
@@ -395,7 +395,7 @@ describe('validateInputValue', () => {
       test({ foo: 123, bar: null }, TestInputObject, [
         {
           error:
-            'Exactly one key must be specified for OneOf type "TestInputObject".',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -409,8 +409,8 @@ describe('validateInputValue', () => {
       test({ bar: null }, TestInputObject, [
         {
           error:
-            'Field "bar" for OneOf type "TestInputObject" must be non-null.',
-          path: [],
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
+          path: ['bar'],
         },
       ]);
     });
@@ -436,7 +436,7 @@ describe('validateInputValue', () => {
         },
         {
           error:
-            'Exactly one key must be specified for OneOf type "TestInputObject".',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -452,7 +452,7 @@ describe('validateInputValue', () => {
         },
         {
           error:
-            'Exactly one key must be specified for OneOf type "TestInputObject".',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -980,7 +980,7 @@ describe('validateInputLiteral', () => {
       test('{ foo: 123, bar: null }', TestInputObject, [
         {
           error:
-            'OneOf Input Object "TestInputObject" must specify exactly one key.',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -990,7 +990,7 @@ describe('validateInputLiteral', () => {
       test('{ bar: null }', TestInputObject, [
         {
           error:
-            'Field "TestInputObject.bar" used for OneOf Input Object must be non-null.',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: ['bar'],
         },
       ]);
@@ -1025,7 +1025,7 @@ describe('validateInputLiteral', () => {
         },
         {
           error:
-            'OneOf Input Object "TestInputObject" must specify exactly one key.',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -1041,7 +1041,7 @@ describe('validateInputLiteral', () => {
         },
         {
           error:
-            'OneOf Input Object "TestInputObject" must specify exactly one key.',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -1087,7 +1087,7 @@ describe('validateInputLiteral', () => {
         },
         {
           error:
-            'OneOf Input Object "TestInputObject" must specify exactly one key.',
+            'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
           path: [],
         },
       ]);
@@ -1105,7 +1105,7 @@ describe('validateInputLiteral', () => {
           },
           {
             error:
-              'OneOf Input Object "TestInputObject" must specify exactly one key.',
+              'Within OneOf Input Object type "TestInputObject", exactly one field must be specified, and the value for that field must be non-null.',
             path: [],
           },
         ],
diff --git a/src/utilities/validateInputValue.ts b/src/utilities/validateInputValue.ts
index abd45fb41e..865a7b81a1 100644
--- a/src/utilities/validateInputValue.ts
+++ b/src/utilities/validateInputValue.ts
@@ -169,7 +169,7 @@ function validateInputValueImpl(
       if (fields.length !== 1) {
         reportInvalidValue(
           onError,
-          `Exactly one key must be specified for OneOf type "${type}".`,
+          getOneOfInputObjectErrorMessage(type),
           path,
         );
       }
@@ -179,8 +179,8 @@ function validateInputValueImpl(
       if (value === null) {
         reportInvalidValue(
           onError,
-          `Field "${field}" for OneOf type "${type}" must be non-null.`,
-          path,
+          getOneOfInputObjectErrorMessage(type),
+          addPath(path, field, type.name),
         );
       }
     }
@@ -437,7 +437,7 @@ function validateInputLiteralImpl(
       if (isNotExactlyOneField) {
         reportInvalidLiteral(
           context.onError,
-          `OneOf Input Object "${type}" must specify exactly one key.`,
+          getOneOfInputObjectErrorMessage(type),
           valueNode,
           path,
         );
@@ -449,7 +449,7 @@ function validateInputLiteralImpl(
         const fieldName = fields[0].name.value;
         reportInvalidLiteral(
           context.onError,
-          `Field "${type}.${fieldName}" used for OneOf Input Object must be non-null.`,
+          getOneOfInputObjectErrorMessage(type),
           valueNode,
           addPath(path, fieldName, undefined),
         );
@@ -532,3 +532,7 @@ function getCaughtErrorMessage(caughtError: unknown): string {
 
   return String(caughtError);
 }
+
+function getOneOfInputObjectErrorMessage(type: GraphQLInputType): string {
+  return `Within OneOf Input Object type "${type}", exactly one field must be specified, and the value for that field must be non-null.`;
+}
diff --git a/src/validation/__tests__/ValuesOfCorrectTypeRule-test.ts b/src/validation/__tests__/ValuesOfCorrectTypeRule-test.ts
index 9631c1ae05..38dbcdcfd5 100644
--- a/src/validation/__tests__/ValuesOfCorrectTypeRule-test.ts
+++ b/src/validation/__tests__/ValuesOfCorrectTypeRule-test.ts
@@ -1147,7 +1147,7 @@ describe('Validate: Values of correct type', () => {
       `).toDeepEqual([
         {
           message:
-            'Field "OneOfInput.stringField" used for OneOf Input Object must be non-null.',
+            'Within OneOf Input Object type "OneOfInput", exactly one field must be specified, and the value for that field must be non-null.',
           locations: [{ line: 4, column: 37 }],
         },
       ]);
@@ -1163,7 +1163,7 @@ describe('Validate: Values of correct type', () => {
       `).toDeepEqual([
         {
           message:
-            'OneOf Input Object "OneOfInput" must specify exactly one key.',
+            'Within OneOf Input Object type "OneOfInput", exactly one field must be specified, and the value for that field must be non-null.',
           locations: [{ line: 4, column: 37 }],
         },
       ]);