diff --git a/mypy/build.py b/mypy/build.py
index 4f22e0703d97..810116df5e02 100644
--- a/mypy/build.py
+++ b/mypy/build.py
@@ -504,6 +504,9 @@ def load_plugins(
     """
     custom_plugins, snapshot = load_plugins_from_config(options, errors, stdout)
 
+    if options._on_plugins_loaded is not None:
+        options._on_plugins_loaded()
+
     custom_plugins += extra_plugins
 
     default_plugin: Plugin = DefaultPlugin(options)
diff --git a/mypy/config_parser.py b/mypy/config_parser.py
index 5f08f342241e..2bfd2a1e2eef 100644
--- a/mypy/config_parser.py
+++ b/mypy/config_parser.py
@@ -8,8 +8,6 @@
 import sys
 from io import StringIO
 
-from mypy.errorcodes import error_codes
-
 if sys.version_info >= (3, 11):
     import tomllib
 else:
@@ -87,15 +85,6 @@ def complain(x: object, additional_info: str = "") -> Never:
         complain(v)
 
 
-def validate_codes(codes: list[str]) -> list[str]:
-    invalid_codes = set(codes) - set(error_codes.keys())
-    if invalid_codes:
-        raise argparse.ArgumentTypeError(
-            f"Invalid error code(s): {', '.join(sorted(invalid_codes))}"
-        )
-    return codes
-
-
 def validate_package_allow_list(allow_list: list[str]) -> list[str]:
     for p in allow_list:
         msg = f"Invalid allow list entry: {p}"
@@ -209,8 +198,8 @@ def split_commas(value: str) -> list[str]:
         [p.strip() for p in split_commas(s)]
     ),
     "enable_incomplete_feature": lambda s: [p.strip() for p in split_commas(s)],
-    "disable_error_code": lambda s: validate_codes([p.strip() for p in split_commas(s)]),
-    "enable_error_code": lambda s: validate_codes([p.strip() for p in split_commas(s)]),
+    "disable_error_code": lambda s: [p.strip() for p in split_commas(s)],
+    "enable_error_code": lambda s: [p.strip() for p in split_commas(s)],
     "package_root": lambda s: [p.strip() for p in split_commas(s)],
     "cache_dir": expand_path,
     "python_executable": expand_path,
@@ -234,8 +223,8 @@ def split_commas(value: str) -> list[str]:
         "always_false": try_split,
         "untyped_calls_exclude": lambda s: validate_package_allow_list(try_split(s)),
         "enable_incomplete_feature": try_split,
-        "disable_error_code": lambda s: validate_codes(try_split(s)),
-        "enable_error_code": lambda s: validate_codes(try_split(s)),
+        "disable_error_code": lambda s: try_split(s),
+        "enable_error_code": lambda s: try_split(s),
         "package_root": try_split,
         "exclude": str_or_array_as_list,
         "packages": try_split,
diff --git a/mypy/main.py b/mypy/main.py
index 0f70eb41bb14..c0b9c0ea1427 100644
--- a/mypy/main.py
+++ b/mypy/main.py
@@ -1456,9 +1456,16 @@ def set_strict_flags() -> None:
     validate_package_allow_list(options.untyped_calls_exclude)
     validate_package_allow_list(options.deprecated_calls_exclude)
 
-    options.process_error_codes(error_callback=parser.error)
     options.process_incomplete_features(error_callback=parser.error, warning_callback=print)
 
+    def on_plugins_loaded() -> None:
+        # Processing error codes after plugins have loaded since plugins may
+        # register custom error codes that we don't know about until plugins
+        # have loaded.
+        options.process_error_codes(error_callback=parser.error)
+
+    options._on_plugins_loaded = on_plugins_loaded
+
     # Compute absolute path for custom typeshed (if present).
     if options.custom_typeshed_dir is not None:
         options.abs_custom_typeshed_dir = os.path.abspath(options.custom_typeshed_dir)
diff --git a/mypy/options.py b/mypy/options.py
index ad4b26cca095..231c13a348d2 100644
--- a/mypy/options.py
+++ b/mypy/options.py
@@ -416,6 +416,8 @@ def __init__(self) -> None:
         # preserving manual tweaks to generated C file)
         self.mypyc_skip_c_generation = False
 
+        self._on_plugins_loaded: Callable[[], None] | None = None
+
     def use_lowercase_names(self) -> bool:
         warnings.warn(
             "options.use_lowercase_names() is deprecated and will be removed in a future version",
diff --git a/mypy/test/teststubtest.py b/mypy/test/teststubtest.py
index 28263e20099d..800f522d90a0 100644
--- a/mypy/test/teststubtest.py
+++ b/mypy/test/teststubtest.py
@@ -12,6 +12,8 @@
 from collections.abc import Iterator
 from typing import Any, Callable
 
+from pytest import raises
+
 import mypy.stubtest
 from mypy import build, nodes
 from mypy.modulefinder import BuildSource
@@ -171,7 +173,12 @@ def build_helper(source: str) -> build.BuildResult:
 
 
 def run_stubtest_with_stderr(
-    stub: str, runtime: str, options: list[str], config_file: str | None = None
+    stub: str,
+    runtime: str,
+    options: list[str],
+    config_file: str | None = None,
+    output: io.StringIO | None = None,
+    outerr: io.StringIO | None = None,
 ) -> tuple[str, str]:
     with use_tmp_dir(TEST_MODULE_NAME) as tmp_dir:
         with open("builtins.pyi", "w") as f:
@@ -188,8 +195,8 @@ def run_stubtest_with_stderr(
             with open(f"{TEST_MODULE_NAME}_config.ini", "w") as f:
                 f.write(config_file)
             options = options + ["--mypy-config-file", f"{TEST_MODULE_NAME}_config.ini"]
-        output = io.StringIO()
-        outerr = io.StringIO()
+        output = io.StringIO() if output is None else output
+        outerr = io.StringIO() if outerr is None else outerr
         with contextlib.redirect_stdout(output), contextlib.redirect_stderr(outerr):
             test_stubs(parse_options([TEST_MODULE_NAME] + options), use_builtins_fixtures=True)
     filtered_output = remove_color_code(
@@ -2888,14 +2895,20 @@ def test_config_file_error_codes_invalid(self) -> None:
         runtime = "temp = 5\n"
         stub = "temp: int\n"
         config_file = "[mypy]\ndisable_error_code = not-a-valid-name\n"
-        output, outerr = run_stubtest_with_stderr(
-            stub=stub, runtime=runtime, options=[], config_file=config_file
-        )
-        assert output == "Success: no issues found in 1 module\n"
-        assert outerr == (
-            "test_module_config.ini: [mypy]: disable_error_code: "
-            "Invalid error code(s): not-a-valid-name\n"
-        )
+        output = io.StringIO()
+        outerr = io.StringIO()
+        with raises(SystemExit):
+            run_stubtest_with_stderr(
+                stub=stub,
+                runtime=runtime,
+                options=[],
+                config_file=config_file,
+                output=output,
+                outerr=outerr,
+            )
+
+        assert output.getvalue() == "error: Invalid error code(s): not-a-valid-name\n"
+        assert outerr.getvalue() == ""
 
     def test_config_file_wrong_incomplete_feature(self) -> None:
         runtime = "x = 1\n"
diff --git a/test-data/unit/check-plugin-error-codes.test b/test-data/unit/check-plugin-error-codes.test
new file mode 100644
index 000000000000..95789477977e
--- /dev/null
+++ b/test-data/unit/check-plugin-error-codes.test
@@ -0,0 +1,32 @@
+[case testCustomErrorCodeFromPluginIsTargetable]
+# flags: --config-file tmp/mypy.ini --show-error-codes
+
+def main() -> None:
+    return
+main() # E: Custom error  [custom]
+
+[file mypy.ini]
+\[mypy]
+plugins=<ROOT>/test-data/unit/plugins/custom_errorcode.py
+
+[case testCustomErrorCodeCanBeDisabled]
+# flags: --config-file tmp/mypy.ini --show-error-codes --disable-error-code=custom
+
+def main() -> None:
+    return
+main()  # no output expected when disabled
+
+[file mypy.ini]
+\[mypy]
+plugins=<ROOT>/test-data/unit/plugins/custom_errorcode.py
+
+[case testCustomErrorCodeCanBeReenabled]
+# flags: --config-file tmp/mypy.ini --show-error-codes --disable-error-code=custom --enable-error-code=custom
+
+def main() -> None:
+    return
+main() # E: Custom error  [custom]
+
+[file mypy.ini]
+\[mypy]
+plugins=<ROOT>/test-data/unit/plugins/custom_errorcode.py