diff --git a/mypy/stubgen.py b/mypy/stubgen.py
index fe90c3d256b7..e312e7209e26 100755
--- a/mypy/stubgen.py
+++ b/mypy/stubgen.py
@@ -48,6 +48,7 @@
 import sys
 import traceback
 from collections.abc import Iterable, Iterator
+from functools import cache
 from typing import Final
 
 import mypy.build
@@ -126,7 +127,11 @@
 from mypy.semanal_shared import find_dataclass_transform_spec
 from mypy.sharedparse import MAGIC_METHODS_POS_ARGS_ONLY
 from mypy.stubdoc import ArgSig, FunctionSig
-from mypy.stubgenc import InspectionStubGenerator, generate_stub_for_c_module
+from mypy.stubgenc import (
+    ExternalSignatureGenerator,
+    InspectionStubGenerator,
+    generate_stub_for_c_module,
+)
 from mypy.stubutil import (
     TYPING_BUILTIN_REPLACEMENTS,
     BaseStubGenerator,
@@ -1872,7 +1877,8 @@ def generate_stubs(options: Options) -> None:
                 all_modules=all_module_names,
             )
 
-    # Separately analyse C modules using different logic.
+    # Reuse the external signature index for C modules in this invocation.
+    load_doc_sigs = cache(ExternalSignatureGenerator.from_doc_dir)
     for mod in c_modules:
         if any(py_mod.module.startswith(mod.module + ".") for py_mod in all_modules):
             target = mod.module.replace(".", "/") + "/__init__.pyi"
@@ -1886,6 +1892,7 @@ def generate_stubs(options: Options) -> None:
                 target,
                 known_modules=all_module_names,
                 doc_dir=options.doc_dir,
+                load_doc_sigs=load_doc_sigs,
                 include_private=options.include_private,
                 export_less=options.export_less,
                 include_docstrings=options.include_docstrings,
diff --git a/mypy/stubgenc.py b/mypy/stubgenc.py
index ba312481c51c..e2ae8aaab2ff 100755
--- a/mypy/stubgenc.py
+++ b/mypy/stubgenc.py
@@ -150,6 +150,7 @@ def generate_stub_for_c_module(
     known_modules: list[str],
     doc_dir: str = "",
     *,
+    load_doc_sigs: Callable[[str], ExternalSignatureGenerator] | None = None,
     include_private: bool = False,
     export_less: bool = False,
     include_docstrings: bool = False,
@@ -174,6 +175,7 @@ def generate_stub_for_c_module(
         module_name,
         known_modules,
         doc_dir,
+        load_doc_sigs=load_doc_sigs,
         include_private=include_private,
         export_less=export_less,
         include_docstrings=include_docstrings,
@@ -243,8 +245,11 @@ def __init__(
         export_less: bool = False,
         include_docstrings: bool = False,
         module: ModuleType | None = None,
+        *,
+        load_doc_sigs: Callable[[str], ExternalSignatureGenerator] | None = None,
     ) -> None:
         self.doc_dir = doc_dir
+        self._load_doc_sigs = load_doc_sigs or ExternalSignatureGenerator.from_doc_dir
         if module is None:
             self.module = importlib.import_module(module_name)
         else:
@@ -397,7 +402,7 @@ def get_sig_generators(self) -> list[SignatureGenerator]:
             sig_generators: list[SignatureGenerator] = [DocstringSignatureGenerator()]
             if self.doc_dir:
                 # Collect info from docs (if given). Always check these first.
-                sig_generators.insert(0, ExternalSignatureGenerator.from_doc_dir(self.doc_dir))
+                sig_generators.insert(0, self._load_doc_sigs(self.doc_dir))
             return sig_generators
 
     def strip_or_import(self, type_name: str) -> str:
diff --git a/mypy/test/teststubgen.py b/mypy/test/teststubgen.py
index b5cdbf479f1c..c3f5552e3be4 100644
--- a/mypy/test/teststubgen.py
+++ b/mypy/test/teststubgen.py
@@ -7,8 +7,10 @@
 import sys
 import tempfile
 import unittest
+from pathlib import Path
 from types import ModuleType
 from typing import Any
+from unittest.mock import patch
 
 import pytest
 
@@ -35,7 +37,7 @@
     mypy_options,
     parse_options,
 )
-from mypy.stubgenc import InspectionStubGenerator, infer_c_method_args
+from mypy.stubgenc import ExternalSignatureGenerator, InspectionStubGenerator, infer_c_method_args
 from mypy.stubutil import (
     ClassInfo,
     FunctionContext,
@@ -120,6 +122,25 @@ def test_module_not_found(self) -> None:
                 sys.stdout = sys.__stdout__
                 os.chdir(current)
 
+    def test_doc_dir_reused_within_one_invocation(self) -> None:
+        with tempfile.TemporaryDirectory() as tmp:
+            doc = Path(tmp, "functions.rst")
+            output = Path(tmp, "out")
+            options = parse_options(
+                ["--doc-dir", tmp, "-m", "math", "-m", "cmath", "-o", str(output)]
+            )
+            with patch.object(
+                ExternalSignatureGenerator,
+                "from_doc_dir",
+                wraps=ExternalSignatureGenerator.from_doc_dir,
+            ) as load:
+                for arg in ["first_argument", "updated_argument"]:
+                    doc.write_text(f".. function:: sqrt({arg})\n")
+                    generate_stubs(options)
+                    for module in ["math", "cmath"]:
+                        assert f"def sqrt({arg}" in (output / f"{module}.pyi").read_text()
+                assert load.call_count == 2
+
     def make_file(self, *path: str, content: str = "") -> None:
         file = os.path.join(*path)
         with open(file, "w") as f: