diff --git a/packages/react-dom/src/__tests__/ReactDOMComponent-test.js b/packages/react-dom/src/__tests__/ReactDOMComponent-test.js
index 2c40743854c36..4414dd37e33ae 100644
--- a/packages/react-dom/src/__tests__/ReactDOMComponent-test.js
+++ b/packages/react-dom/src/__tests__/ReactDOMComponent-test.js
@@ -1709,15 +1709,25 @@ describe('ReactDOMComponent', () => {
     it('should warn about incorrect casing on event handlers (ssr)', () => {
       spyOnDev(console, 'error');
       ReactDOMServer.renderToString(
-        React.createElement('input', {type: 'text', onclick: '1'}),
+        React.createElement('input', {type: 'text', oninput: '1'}),
       );
       ReactDOMServer.renderToString(
         React.createElement('input', {type: 'text', onKeydown: '1'}),
       );
       if (__DEV__) {
-        expect(console.error.calls.count()).toBe(2);
-        expect(console.error.calls.argsFor(0)[0]).toContain('onClick');
-        expect(console.error.calls.argsFor(1)[0]).toContain('onKeyDown');
+        expect(console.error.calls.count()).toBe(1);
+        expect(console.error.calls.argsFor(0)[0]).toContain(
+          'Invalid event handler property `oninput`. ' +
+            'React events use the camelCase naming convention, ' +
+            // Note: we don't know the right event name so we
+            // use a generic one (onClick) as a suggestion.
+            // This is because we don't bundle the event system
+            // on the server.
+            'for example `onClick`.',
+        );
+        // We can't warn for `onKeydown` on the server because
+        // there is no way tell if this is a valid event or not
+        // without access to the event system (which we don't bundle).
       }
     });
 
@@ -1735,14 +1745,14 @@ describe('ReactDOMComponent', () => {
     it('should warn about incorrect casing on event handlers', () => {
       spyOnDev(console, 'error');
       ReactTestUtils.renderIntoDocument(
-        React.createElement('input', {type: 'text', onclick: '1'}),
+        React.createElement('input', {type: 'text', oninput: '1'}),
       );
       ReactTestUtils.renderIntoDocument(
         React.createElement('input', {type: 'text', onKeydown: '1'}),
       );
       if (__DEV__) {
         expect(console.error.calls.count()).toBe(2);
-        expect(console.error.calls.argsFor(0)[0]).toContain('onClick');
+        expect(console.error.calls.argsFor(0)[0]).toContain('onInput');
         expect(console.error.calls.argsFor(1)[0]).toContain('onKeyDown');
       }
     });
@@ -1860,15 +1870,20 @@ describe('ReactDOMComponent', () => {
     it('gives source code refs for unknown prop warning (ssr)', () => {
       spyOnDev(console, 'error');
       ReactDOMServer.renderToString(<div class="paladin" />);
-      ReactDOMServer.renderToString(<input type="text" onclick="1" />);
+      ReactDOMServer.renderToString(<input type="text" oninput="1" />);
       if (__DEV__) {
         expect(console.error.calls.count()).toBe(2);
         expect(normalizeCodeLocInfo(console.error.calls.argsFor(0)[0])).toBe(
           'Warning: Invalid DOM property `class`. Did you mean `className`?\n    in div (at **)',
         );
         expect(normalizeCodeLocInfo(console.error.calls.argsFor(1)[0])).toBe(
-          'Warning: Invalid event handler property `onclick`. Did you mean ' +
-            '`onClick`?\n    in input (at **)',
+          'Warning: Invalid event handler property `oninput`. ' +
+            // Note: we don't know the right event name so we
+            // use a generic one (onClick) as a suggestion.
+            // This is because we don't bundle the event system
+            // on the server.
+            'React events use the camelCase naming convention, for example `onClick`.' +
+            '\n    in input (at **)',
         );
       }
     });
diff --git a/packages/react-dom/src/client/ReactDOMFiberComponent.js b/packages/react-dom/src/client/ReactDOMFiberComponent.js
index e6ff7e7c92cb2..1ed31563d3395 100644
--- a/packages/react-dom/src/client/ReactDOMFiberComponent.js
+++ b/packages/react-dom/src/client/ReactDOMFiberComponent.js
@@ -67,7 +67,7 @@ if (__DEV__) {
   var validatePropertiesInDevelopment = function(type, props) {
     validateARIAProperties(type, props);
     validateInputProperties(type, props);
-    validateUnknownProperties(type, props);
+    validateUnknownProperties(type, props, /* canUseEventSystem */ true);
   };
 
   // HTML parsing normalizes CR and CRLF to LF.
diff --git a/packages/react-dom/src/server/ReactPartialRenderer.js b/packages/react-dom/src/server/ReactPartialRenderer.js
index bf63c063f5942..60f03527653ae 100644
--- a/packages/react-dom/src/server/ReactPartialRenderer.js
+++ b/packages/react-dom/src/server/ReactPartialRenderer.js
@@ -54,7 +54,7 @@ if (__DEV__) {
   var validatePropertiesInDevelopment = function(type, props) {
     validateARIAProperties(type, props);
     validateInputProperties(type, props);
-    validateUnknownProperties(type, props);
+    validateUnknownProperties(type, props, /* canUseEventSystem */ false);
   };
 
   var describeStackFrame = function(element): string {
diff --git a/packages/react-dom/src/shared/ReactDOMUnknownPropertyHook.js b/packages/react-dom/src/shared/ReactDOMUnknownPropertyHook.js
index 7dd26a57bfc0b..f02d728cf4acc 100644
--- a/packages/react-dom/src/shared/ReactDOMUnknownPropertyHook.js
+++ b/packages/react-dom/src/shared/ReactDOMUnknownPropertyHook.js
@@ -7,7 +7,6 @@
 
 import {
   registrationNameModules,
-  plugins,
   possibleRegistrationNames,
 } from 'events/EventPluginRegistry';
 import {ReactDebugCurrentFrame} from 'shared/ReactGlobalSharedState';
@@ -30,51 +29,72 @@ function getStackAddendum() {
 if (__DEV__) {
   var warnedProperties = {};
   var hasOwnProperty = Object.prototype.hasOwnProperty;
-  var EVENT_NAME_REGEX = /^on[A-Z]/;
+  var EVENT_NAME_REGEX = /^on[a-zA-Z]/;
+  var INVALID_EVENT_NAME_REGEX = /^on[a-z]/;
   var rARIA = new RegExp('^(aria)-[' + ATTRIBUTE_NAME_CHAR + ']*$');
   var rARIACamel = new RegExp('^(aria)[A-Z][' + ATTRIBUTE_NAME_CHAR + ']*$');
 
-  var validateProperty = function(tagName, name, value) {
+  var validateProperty = function(tagName, name, value, canUseEventSystem) {
     if (hasOwnProperty.call(warnedProperties, name) && warnedProperties[name]) {
       return true;
     }
 
-    if (registrationNameModules.hasOwnProperty(name)) {
-      return true;
-    }
-
-    if (plugins.length === 0 && EVENT_NAME_REGEX.test(name)) {
-      // If no event plugins have been injected, we might be in a server environment.
-      // Don't check events in this case.
-      return true;
-    }
-
     var lowerCasedName = name.toLowerCase();
-    var registrationName = possibleRegistrationNames.hasOwnProperty(
-      lowerCasedName,
-    )
-      ? possibleRegistrationNames[lowerCasedName]
-      : null;
-
-    if (registrationName != null) {
+    if (lowerCasedName === 'onfocusin' || lowerCasedName === 'onfocusout') {
       warning(
         false,
-        'Invalid event handler property `%s`. Did you mean `%s`?%s',
-        name,
-        registrationName,
-        getStackAddendum(),
+        'React uses onFocus and onBlur instead of onFocusIn and onFocusOut. ' +
+          'All React events are normalized to bubble, so onFocusIn and onFocusOut ' +
+          'are not needed/supported by React.',
       );
       warnedProperties[name] = true;
       return true;
     }
 
-    if (lowerCasedName.indexOf('on') === 0 && lowerCasedName.length > 2) {
-      warning(
-        false,
-        'Unknown event handler property `%s`. It will be ignored.%s',
-        name,
-        getStackAddendum(),
-      );
+    // We can't rely on the event system being injected on the server.
+    if (canUseEventSystem) {
+      if (registrationNameModules.hasOwnProperty(name)) {
+        return true;
+      }
+      var registrationName = possibleRegistrationNames.hasOwnProperty(
+        lowerCasedName,
+      )
+        ? possibleRegistrationNames[lowerCasedName]
+        : null;
+      if (registrationName != null) {
+        warning(
+          false,
+          'Invalid event handler property `%s`. Did you mean `%s`?%s',
+          name,
+          registrationName,
+          getStackAddendum(),
+        );
+        warnedProperties[name] = true;
+        return true;
+      }
+      if (lowerCasedName.indexOf('on') === 0 && lowerCasedName.length > 2) {
+        warning(
+          false,
+          'Unknown event handler property `%s`. It will be ignored.%s',
+          name,
+          getStackAddendum(),
+        );
+        warnedProperties[name] = true;
+        return true;
+      }
+    } else if (EVENT_NAME_REGEX.test(name)) {
+      // If no event plugins have been injected, we are in a server environment.
+      // So we can't tell if the event name is correct for sure, but we can filter
+      // out known bad ones like `onclick`. We can't suggest a specific replacement though.
+      if (INVALID_EVENT_NAME_REGEX.test(name)) {
+        warning(
+          false,
+          'Invalid event handler property `%s`. ' +
+            'React events use the camelCase naming convention, for example `onClick`.%s',
+          name,
+          getStackAddendum(),
+        );
+      }
       warnedProperties[name] = true;
       return true;
     }
@@ -84,17 +104,6 @@ if (__DEV__) {
       return true;
     }
 
-    if (lowerCasedName === 'onfocusin' || lowerCasedName === 'onfocusout') {
-      warning(
-        false,
-        'React uses onFocus and onBlur instead of onFocusIn and onFocusOut. ' +
-          'All React events are normalized to bubble, so onFocusIn and onFocusOut ' +
-          'are not needed/supported by React.',
-      );
-      warnedProperties[name] = true;
-      return true;
-    }
-
     if (lowerCasedName === 'innerhtml') {
       warning(
         false,
@@ -233,10 +242,10 @@ if (__DEV__) {
   };
 }
 
-var warnUnknownProperties = function(type, props) {
+var warnUnknownProperties = function(type, props, canUseEventSystem) {
   var unknownProps = [];
   for (var key in props) {
-    var isValid = validateProperty(type, key, props[key]);
+    var isValid = validateProperty(type, key, props[key], canUseEventSystem);
     if (!isValid) {
       unknownProps.push(key);
     }
@@ -266,9 +275,9 @@ var warnUnknownProperties = function(type, props) {
   }
 };
 
-export function validateProperties(type, props) {
+export function validateProperties(type, props, canUseEventSystem) {
   if (isCustomComponent(type, props)) {
     return;
   }
-  warnUnknownProperties(type, props);
+  warnUnknownProperties(type, props, canUseEventSystem);
 }