diff --git a/changelog/2720.bugfix.rst b/changelog/2720.bugfix.rst
new file mode 100644
index 00000000000..ac947c74600
--- /dev/null
+++ b/changelog/2720.bugfix.rst
@@ -0,0 +1,8 @@
+Plugins now contribute their own hookspecs via :hook:`pytest_addhooks` as soon as they are
+registered, instead of only when a :class:`~pytest.Config` parses a command line.
+
+Previously a :class:`~pytest.PytestPluginManager` obtained outside a full pytest run - for
+example from ``_pytest.config.get_plugin_manager()``, which is documented for integration
+with other tools - never called :hook:`pytest_addhooks` on the plugins registered with it.
+Such a plugin's own hook implementations were then rejected with
+``PluginValidationError: unknown hook ...``.
diff --git a/src/_pytest/config/__init__.py b/src/_pytest/config/__init__.py
index c7bd3e1afab..951e7098558 100644
--- a/src/_pytest/config/__init__.py
+++ b/src/_pytest/config/__init__.py
@@ -529,6 +529,10 @@ def __init__(self) -> None:
 
         self.add_hookspecs(_pytest.hookspec)
         self.register(self)
+        # Historic, so that plugins registered later - which is all of them -
+        # get to contribute their own hookspecs as they are registered, rather
+        # than only if and when a Config gets around to parsing a command line.
+        self.hook.pytest_addhooks.call_historic(kwargs=dict(pluginmanager=self))
         if os.environ.get("PYTEST_DEBUG"):
             err: IO[str] = sys.stderr
             encoding: str = getattr(err, "encoding", "utf8")
@@ -1634,10 +1638,6 @@ def parse(self, args: list[str], addopts: bool = True) -> None:
             "can only parse cmdline args at most once per Config object"
         )
 
-        self.hook.pytest_addhooks.call_historic(
-            kwargs=dict(pluginmanager=self.pluginmanager)
-        )
-
         if addopts:
             env_addopts = os.environ.get("PYTEST_ADDOPTS", "")
             if len(env_addopts):
diff --git a/testing/test_pluginmanager.py b/testing/test_pluginmanager.py
index 03887de61d9..9e2759a84bf 100644
--- a/testing/test_pluginmanager.py
+++ b/testing/test_pluginmanager.py
@@ -46,10 +46,6 @@ def pytest_myhook(xyz):
         """
         )
         config = _config_for_test
-        pm = config.pluginmanager
-        pm.hook.pytest_addhooks.call_historic(
-            kwargs=dict(pluginmanager=config.pluginmanager)
-        )
         config.pluginmanager._importconftest(
             conf,
             importmode="prepend",
@@ -60,6 +56,27 @@ def pytest_myhook(xyz):
         res = config.hook.pytest_myhook(xyz=10)
         assert res == [11]
 
+    def test_addhooks_on_registration(self, pytestpm: PytestPluginManager) -> None:
+        """A plugin contributes its hookspecs when it is registered, not when
+        some Config gets around to parsing a command line (#2720)."""
+
+        class NewHooks:
+            def pytest_myhook(self, xyz):
+                """New hook"""
+
+        class Plugin:
+            def pytest_addhooks(self, pluginmanager):
+                pluginmanager.add_hookspecs(NewHooks)
+
+            def pytest_myhook(self, xyz):
+                return xyz + 1
+
+        pytestpm.register(Plugin())
+
+        assert pytestpm.hook.pytest_myhook.has_spec()
+        pytestpm.check_pending()
+        assert pytestpm.hook.pytest_myhook(xyz=10) == [11]
+
     def test_addhooks_nohooks(self, pytester: Pytester) -> None:
         pytester.makeconftest(
             """