diff --git a/client/src/mvc/tool/tool-form.js b/client/src/mvc/tool/tool-form.js
index 43b89ccfca2..e1bb04265ec 100644
--- a/client/src/mvc/tool/tool-form.js
+++ b/client/src/mvc/tool/tool-form.js
@@ -356,7 +356,7 @@ const View = Backbone.View.extend({
                 continue;
             }
             if (!input_def.optional && input_value == null && input_def.type != "hidden") {
-                this.form.highlight(input_id);
+                this.form.highlight(input_id, "This input requires a value.");
                 return false;
             }
             if (input_field.validate) {
diff --git a/lib/galaxy/tool_util/linters/inputs.py b/lib/galaxy/tool_util/linters/inputs.py
index ff905a1a0df..7446653410b 100644
--- a/lib/galaxy/tool_util/linters/inputs.py
+++ b/lib/galaxy/tool_util/linters/inputs.py
@@ -44,6 +44,11 @@ def lint_inputs(tool_xml, lint_ctx):
             if dynamic_options is None and len(select_options) == 0:
                 lint_ctx.warn(f"No options defined for select [{param_name}]")
 
+            if param_attrib.get("display") == "checkboxes":
+                if not string_as_bool(param_attrib.get("multiple", "false")):
+                    lint_ctx.error(f'Select [{param_name}] `display="checkboxes"` is incompatible with `multiple="false"`, remove the `display` attribute')
+                if not string_as_bool(param_attrib.get("optional", "false")):
+                    lint_ctx.error(f'Select [{param_name}] `display="checkboxes"` is incompatible with `optional="false"`, remove the `display` attribute')
             if param_attrib.get("display") == "radio":
                 if string_as_bool(param_attrib.get("multiple", "false")):
                     lint_ctx.error(f'Select [{param_name}] display="radio" is incompatible with multiple="true"')
diff --git a/lib/galaxy/tool_util/xsd/galaxy.xsd b/lib/galaxy/tool_util/xsd/galaxy.xsd
index 86e696ef871..269f9ba45d8 100644
--- a/lib/galaxy/tool_util/xsd/galaxy.xsd
+++ b/lib/galaxy/tool_util/xsd/galaxy.xsd
@@ -2888,7 +2888,8 @@ is still the column index. Used only when the ``type`` attribute value is
         <xs:attribute name="display" type="DisplayType">
           <xs:annotation>
             <xs:documentation xml:lang="en">Render a select list as a set of
-checkboxes (``checkboxes``) or radio buttons (``radio``; note this is
+checkboxes (``checkboxes``; note this is incompatible with ``multiple="false"``
+and ``optional="false"``) or radio buttons (``radio``; note this is
 incompatible with ``multiple="true"`` and ``optional="true"``). Defaults to a
 drop-down menu select list. Used only when the ``type`` attribute value is
 ``select``.</xs:documentation>
diff --git a/test/unit/tool_util/test_tool_linters.py b/test/unit/tool_util/test_tool_linters.py
index 16e64a4b000..99036d459fc 100644
--- a/test/unit/tool_util/test_tool_linters.py
+++ b/test/unit/tool_util/test_tool_linters.py
@@ -31,7 +31,14 @@ RADIO_SELECT_INCOMPATIBILITIES = """
     <description>The BWA Mapper</description>
     <version_command interpreter="python">bwa.py --version</version_command>
     <inputs>
-        <param name="radio_select" type="select" display="radio" optional="true" multiple="true"/>
+        <param name="radio_select" type="select" display="radio" optional="true" multiple="true">
+            <option value="1">1</option>
+            <option value="2">2</option>
+        </param>
+        <param name="radio_checkboxes" type="select" display="checkboxes" optional="false" multiple="false">
+            <option value="1">1</option>
+            <option value="2">2</option>
+        </param>
     </inputs>
 </tool>
 """
@@ -51,13 +58,35 @@ SELECT_DUPLICATED_OPTIONS = """
 
 TESTS = [
     (NO_SECTIONS_XML, inputs.lint_inputs, lambda x: 'Found no input parameters.' in x.warn_messages),
-    (NO_WHEN_IN_CONDITIONAL_XML, inputs.lint_inputs, lambda x: "Conditional [labels] no <when /> block found for select option 'none'" in x.warn_messages),
-    (RADIO_SELECT_INCOMPATIBILITIES, inputs.lint_inputs, lambda x: 'Select [radio_select] display="radio" is incompatible with optional="true"' in x.error_messages and 'Select [radio_select] display="radio" is incompatible with multiple="true"' in x.error_messages),
-    (SELECT_DUPLICATED_OPTIONS, inputs.lint_inputs, lambda x: 'Select [select] has multiple options with the same text content' in x.error_messages and 'Select [select] has multiple options with the same value' in x.error_messages),
+    (
+        NO_WHEN_IN_CONDITIONAL_XML, inputs.lint_inputs,
+        lambda x: "Conditional [labels] no <when /> block found for select option 'none'" in x.warn_messages
+    ),
+    (
+        RADIO_SELECT_INCOMPATIBILITIES, inputs.lint_inputs,
+        lambda x:
+            'Select [radio_select] display="radio" is incompatible with optional="true"' in x.error_messages
+            and 'Select [radio_select] display="radio" is incompatible with multiple="true"' in x.error_messages
+            and 'Select [radio_checkboxes] `display="checkboxes"` is incompatible with `optional="false"`, remove the `display` attribute' in x.error_messages
+            and 'Select [radio_checkboxes] `display="checkboxes"` is incompatible with `multiple="false"`, remove the `display` attribute' in x.error_messages
+    ),
+    (
+        SELECT_DUPLICATED_OPTIONS, inputs.lint_inputs,
+        lambda x:
+            'Select [select] has multiple options with the same text content' in x.error_messages
+            and 'Select [select] has multiple options with the same value' in x.error_messages
+    ),
+]
+
+TEST_IDS = [
+    'Lint no sections',
+    'lint no when',
+    'radio select incompatibilities',
+    'select duplicated options'
 ]
 
 
-@pytest.mark.parametrize('tool_xml,lint_func,assert_func', TESTS, ids=['Lint no sections', 'lint no when', 'radio select incompatibilities', 'select duplicated options'])
+@pytest.mark.parametrize('tool_xml,lint_func,assert_func', TESTS, ids=TEST_IDS)
 def test_tool_xml(tool_xml, lint_func, assert_func):
     lint_ctx = LintContext('all')
     tree = etree.ElementTree(element=etree.fromstring(tool_xml))