diff --git a/changelog/7620.bugfix.rst b/changelog/7620.bugfix.rst
new file mode 100644
index 00000000000..d99cc202785
--- /dev/null
+++ b/changelog/7620.bugfix.rst
@@ -0,0 +1,3 @@
+It is now possible to silence :class:`pytest.PytestConfigWarning` messages about unknown configuration keys by using :confval:`filterwarnings`.
+
+Also, multiple keys are combined in a single warning, instead of showing a separate warning per key.
diff --git a/src/_pytest/config/__init__.py b/src/_pytest/config/__init__.py
index 453dd834537..f0cc38914ed 100644
--- a/src/_pytest/config/__init__.py
+++ b/src/_pytest/config/__init__.py
@@ -1127,7 +1127,12 @@ def _preparse(self, args: List[str], addopts: bool = True) -> None:
                 )
             else:
                 raise
-        self._validate_keys()
+
+    @hookimpl(hookwrapper=True)
+    def pytest_collection(self):
+        """Validate invalid ini keys after collection is done."""
+        yield
+        self._validate_config_keys()
 
     def _checkversion(self) -> None:
         import pytest
@@ -1148,9 +1153,13 @@ def _checkversion(self) -> None:
                     % (self.inifile, minver, pytest.__version__,)
                 )
 
-    def _validate_keys(self) -> None:
-        for key in sorted(self._get_unknown_ini_keys()):
-            self._warn_or_fail_if_strict("Unknown config ini key: {}\n".format(key))
+    def _validate_config_keys(self) -> None:
+        keys = sorted(self._get_unknown_ini_keys())
+        if keys:
+            noun = "key" if len(keys) == 1 else "keys"
+            self._warn_or_fail_if_strict(
+                "Unknown config {}: {}".format(noun, ", ".join(keys))
+            )
 
     def _validate_plugins(self) -> None:
         required_plugins = sorted(self.getini("required_plugins"))
@@ -1185,14 +1194,11 @@ def _validate_plugins(self) -> None:
             )
 
     def _warn_or_fail_if_strict(self, message: str) -> None:
+        """Issue a PytestConfigWarning or fail if --strict-config was given"""
         if self.known_args_namespace.strict_config:
             fail(message, pytrace=False)
 
-        from _pytest.warnings import _issue_warning_captured
-
-        _issue_warning_captured(
-            PytestConfigWarning(message), self.hook, stacklevel=3,
-        )
+        warnings.warn(PytestConfigWarning(message))
 
     def _get_unknown_ini_keys(self) -> List[str]:
         parser_inicfg = self._parser._inidict
diff --git a/testing/test_config.py b/testing/test_config.py
index 346edb3304c..35ffcf1b152 100644
--- a/testing/test_config.py
+++ b/testing/test_config.py
@@ -183,10 +183,9 @@ def test_confcutdir(self, testdir):
                 ["unknown_ini", "another_unknown_ini"],
                 [
                     "=*= warnings summary =*=",
-                    "*PytestConfigWarning:*Unknown config ini key: another_unknown_ini",
-                    "*PytestConfigWarning:*Unknown config ini key: unknown_ini",
+                    "*PytestConfigWarning:*Unknown config keys: another_unknown_ini, unknown_ini",
                 ],
-                "Unknown config ini key: another_unknown_ini",
+                "Unknown config keys: another_unknown_ini, unknown_ini",
             ),
             (
                 """
@@ -197,9 +196,9 @@ def test_confcutdir(self, testdir):
                 ["unknown_ini"],
                 [
                     "=*= warnings summary =*=",
-                    "*PytestConfigWarning:*Unknown config ini key: unknown_ini",
+                    "*PytestConfigWarning:*Unknown config key: unknown_ini",
                 ],
-                "Unknown config ini key: unknown_ini",
+                "Unknown config key: unknown_ini",
             ),
             (
                 """
@@ -232,6 +231,7 @@ def test_confcutdir(self, testdir):
             ),
         ],
     )
+    @pytest.mark.filterwarnings("default")
     def test_invalid_ini_keys(
         self, testdir, ini_file_text, invalid_keys, warning_output, exception_text
     ):
@@ -250,10 +250,21 @@ def pytest_addoption(parser):
         result.stdout.fnmatch_lines(warning_output)
 
         if exception_text:
-            with pytest.raises(pytest.fail.Exception, match=exception_text):
-                testdir.runpytest("--strict-config")
-        else:
-            testdir.runpytest("--strict-config")
+            result = testdir.runpytest("--strict-config")
+            result.stdout.fnmatch_lines("INTERNALERROR>*" + exception_text)
+
+    @pytest.mark.filterwarnings("default")
+    def test_silence_unknown_key_warning(self, testdir):
+        testdir.makeini(
+            """
+            [pytest]
+            filterwarnings =
+                ignore:Unknown config key:pytest.PytestConfigWarning
+            foobar=1
+        """
+        )
+        result = testdir.runpytest()
+        result.stdout.no_fnmatch_line("*PytestConfigWarning*")
 
     @pytest.mark.parametrize(
         "ini_file_text, exception_text",