diff --git a/include/pybind11/attr.h b/include/pybind11/attr.h
index 57517fa0..c7ff8714 100644
--- a/include/pybind11/attr.h
+++ b/include/pybind11/attr.h
@@ -179,13 +179,20 @@ struct argument_record {
     const char *name;  ///< Argument name
     const char *descr; ///< Human-readable version of the argument value
     handle value;      ///< Associated Python object
+    // The explicit value_is_nullptr variable is for safety, to unambiguously
+    // distinguish these two cases in all situations:
+    // * value is nullptr on purpose (value_is_nullptr true).
+    // * value is nullptr because of an error condition (value_is_nullptr false).
+    bool value_is_nullptr;
     from_python_policies policies;
 
     argument_record(const char *name,
                     const char *descr,
                     handle value,
+                    bool value_is_nullptr,
                     const from_python_policies &policies)
-        : name(name), descr(descr), value(value), policies(policies) {}
+        : name(name), descr(descr), value(value), value_is_nullptr(value_is_nullptr),
+          policies(policies) {}
 };
 
 /// Internal data structure which holds metadata about a bound function (signature, overloads,
@@ -474,8 +481,11 @@ inline void check_kw_only_arg(const arg &a, function_record *r) {
 
 inline void append_self_arg_if_needed(function_record *r) {
     if (r->is_method && r->args.empty()) {
-        r->args.emplace_back(
-            "self", nullptr, handle(), from_python_policies(/*convert=*/true, /*none=*/false));
+        r->args.emplace_back("self",
+                             nullptr,
+                             handle(),
+                             /*value_is_nullptr=*/false,
+                             from_python_policies(/*convert=*/true, /*none=*/false));
     }
 }
 
@@ -488,6 +498,7 @@ struct process_attribute<arg> : process_attribute_default<arg> {
             a.name,
             nullptr,
             handle(),
+            /*value_is_nullptr=*/false,
             from_python_policies(a.m_policies.rvpp, !a.flag_noconvert, a.flag_none));
 
         check_kw_only_arg(a, r);
@@ -504,10 +515,11 @@ struct process_attribute<arg_v> : process_attribute_default<arg_v> {
             r->args.emplace_back("self",
                                  /*descr=*/nullptr,
                                  /*parent=*/handle(),
+                                 /*value_is_nullptr=*/false,
                                  from_python_policies(/*convert=*/true, /*none=*/false));
         }
 
-        if (!a.value) {
+        if (!a.value && !a.value_is_nullptr) {
 #if defined(PYBIND11_DETAILED_ERROR_MESSAGES)
             std::string descr("'");
             if (a.name) {
@@ -537,6 +549,7 @@ struct process_attribute<arg_v> : process_attribute_default<arg_v> {
             a.name,
             a.descr,
             a.value.inc_ref(),
+            a.value_is_nullptr,
             from_python_policies(a.m_policies.rvpp, !a.flag_noconvert, a.flag_none));
 
         check_kw_only_arg(a, r);
diff --git a/include/pybind11/cast.h b/include/pybind11/cast.h
index 4eb6a1fb..1ff870b2 100644
--- a/include/pybind11/cast.h
+++ b/include/pybind11/cast.h
@@ -1535,6 +1535,8 @@ struct arg : detail::arg_base {
     from_python_policies m_policies;
 };
 
+struct nullptr_default_arg {};
+
 /// \ingroup annotations
 /// Annotation for arguments with values
 struct arg_v : arg {
@@ -1544,6 +1546,16 @@ struct arg_v : arg {
 private:
 #endif
     friend struct arg_base;
+
+    arg_v(arg &&base, nullptr_default_arg, const char *descr = nullptr)
+        : arg(base), value(), value_is_nullptr(true), descr(descr)
+#if defined(PYBIND11_DETAILED_ERROR_MESSAGES)
+          ,
+          type("pybind11::nullptr_default_arg")
+#endif
+    {
+    }
+
     template <typename T>
     arg_v(arg &&base, T &&x, const char *descr = nullptr)
         : arg(base), value(reinterpret_steal<object>(detail::make_caster<T>::cast(
@@ -1587,6 +1599,7 @@ struct arg_v : arg {
 
     /// The default value
     object value;
+    bool value_is_nullptr = false;
     /// The (optional) description of the default value
     const char *descr;
 #if defined(PYBIND11_DETAILED_ERROR_MESSAGES)
diff --git a/include/pybind11/pybind11.h b/include/pybind11/pybind11.h
index 137921a1..3c28829a 100644
--- a/include/pybind11/pybind11.h
+++ b/include/pybind11/pybind11.h
@@ -910,7 +910,7 @@ class cpp_function : public function {
                             break;
                         }
 
-                        if (value) {
+                        if (value || arg_rec.value_is_nullptr) {
                             // If we're at the py::args index then first insert a stub for it to be
                             // replaced later
                             if (func.has_args && call.args.size() == func.nargs_pos) {
diff --git a/tests/test_type_caster_pyobject_ptr.cpp b/tests/test_type_caster_pyobject_ptr.cpp
index 8069f7dc..6bab988f 100644
--- a/tests/test_type_caster_pyobject_ptr.cpp
+++ b/tests/test_type_caster_pyobject_ptr.cpp
@@ -127,4 +127,28 @@ TEST_SUBMODULE(type_caster_pyobject_ptr, m) {
         (void) py::cast(*ptr);
     }
 #endif
+
+    // This test exercises functionality (`py::cast<PyObject *>(handle_nullptr)`)
+    // that is needed indirectly below in py_arg_handle_nullptr.
+    m.def("pyobject_ptr_from_handle_nullptr", []() {
+        py::handle handle_nullptr;
+        if (handle_nullptr.ptr() != nullptr) {
+            return "UNEXPECTED: handle_nullptr.ptr() != nullptr";
+        }
+        auto *pyobject_ptr_from_handle = py::cast<PyObject *>(handle_nullptr);
+        if (pyobject_ptr_from_handle != nullptr) {
+            return "UNEXPECTED: pyobject_ptr_from_handle != nullptr";
+        }
+        return "SUCCESS";
+    });
+
+    m.def(
+        "py_arg_handle_nullptr",
+        [](PyObject *ptr) {
+            if (ptr == nullptr) {
+                return "ptr == nullptr";
+            }
+            return py::detail::obj_class_name(ptr);
+        },
+        py::arg("ptr") = py::nullptr_default_arg());
 }
diff --git a/tests/test_type_caster_pyobject_ptr.py b/tests/test_type_caster_pyobject_ptr.py
index 1f1ece2b..367af458 100644
--- a/tests/test_type_caster_pyobject_ptr.py
+++ b/tests/test_type_caster_pyobject_ptr.py
@@ -102,3 +102,13 @@ def test_return_list_pyobject_ptr_reference():
 def test_type_caster_name_via_incompatible_function_arguments_type_error():
     with pytest.raises(TypeError, match=r"1\. \(arg0: object, arg1: int\) -> None"):
         m.pass_pyobject_ptr_and_int(ValueHolder(101), ValueHolder(202))
+
+
+def test_pyobject_ptr_from_handle_nullptr():
+    assert m.pyobject_ptr_from_handle_nullptr() == "SUCCESS"
+
+
+def test_py_arg_handle_nullptr():
+    assert m.py_arg_handle_nullptr(None) == "NoneType"
+    assert m.py_arg_handle_nullptr([]) == "list"
+    assert m.py_arg_handle_nullptr() == "ptr == nullptr"