diff --git a/poetry.lock b/poetry.lock
index 1cb6c86aeb9..51d204b2cf2 100644
--- a/poetry.lock
+++ b/poetry.lock
@@ -1570,6 +1570,19 @@ files = [
     {file = "trove_classifiers-2024.10.21.16.tar.gz", hash = "sha256:17cbd055d67d5e9d9de63293a8732943fabc21574e4c7b74edf112b4928cf5f3"},
 ]
 
+[[package]]
+name = "truststore"
+version = "0.10.0"
+description = "Verify certificates using native system trust stores"
+optional = false
+python-versions = ">=3.10"
+groups = ["main"]
+markers = "python_version >= \"3.10\""
+files = [
+    {file = "truststore-0.10.0-py3-none-any.whl", hash = "sha256:b3798548e421ffe2ca2a6217cca49e7a17baf40b72d86a5505dc7d701e77d15b"},
+    {file = "truststore-0.10.0.tar.gz", hash = "sha256:5da347c665714fdfbd46f738c823fe9f0d8775e41ac5fb94f325749091187896"},
+]
+
 [[package]]
 name = "types-requests"
 version = "2.32.0.20241016"
@@ -1735,4 +1748,4 @@ type = ["pytest-mypy"]
 [metadata]
 lock-version = "2.1"
 python-versions = ">=3.9,<4.0"
-content-hash = "308952b9d3e6645aa1a55c5c021949e2300dd78a8f0049cdf2814785e1196dc5"
+content-hash = "8b5159eb8fa3222d9b096fdd0efd2fd042fd016a8359f47981e8444680e83dbf"
diff --git a/pyproject.toml b/pyproject.toml
index e6037c56bb2..bf01c0e7b66 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -25,6 +25,7 @@ dependencies = [
     "tomlkit (>=0.11.4,<1.0.0)",
     # trove-classifiers uses calver, so version is unclamped
     "trove-classifiers (>=2022.5.19)",
+    "truststore (>=0.10.0,<1.0.0) ; python_version >= '3.10'",
     "virtualenv (>=20.26.6,<21.0.0)",
     "xattr (>=1.0.0,<2.0.0) ; sys_platform == 'darwin'",
 ]
@@ -187,6 +188,7 @@ module = [
     'shellingham.*',
     'virtualenv.*',
     'xattr.*',
+    'truststore.*' # not available on Python < 3.10
 ]
 ignore_missing_imports = true
 
diff --git a/src/poetry/config/config.py b/src/poetry/config/config.py
index 22906db6a19..f4634a8f838 100644
--- a/src/poetry/config/config.py
+++ b/src/poetry/config/config.py
@@ -136,6 +136,8 @@ class Config:
         "keyring": {
             "enabled": True,
         },
+        # TODO: Flip to default True on the next release after dropping Python 3.9
+        "system-truststore": False,
     }
 
     def __init__(self, use_environment: bool = True) -> None:
@@ -303,6 +305,7 @@ def _get_normalizer(name: str) -> Callable[[str], Any]:
             "solver.lazy-wheel",
             "system-git-client",
             "keyring.enabled",
+            "system-truststore",
         }:
             return boolean_normalizer
 
diff --git a/src/poetry/console/application.py b/src/poetry/console/application.py
index 89f78bf0819..1630020d9b6 100644
--- a/src/poetry/console/application.py
+++ b/src/poetry/console/application.py
@@ -226,6 +226,7 @@ def _run(self, io: IO) -> int:
         self._configure_custom_application_options(io)
 
         self._load_plugins(io)
+        self._load_system_truststore()
 
         with directory(self._working_directory):
             exit_code: int = super()._run(io)
@@ -441,6 +442,15 @@ def _load_plugins(self, io: IO) -> None:
 
         self._plugins_loaded = True
 
+    @staticmethod
+    def _load_system_truststore() -> None:
+        from poetry.utils.ssl_truststore import is_truststore_enabled
+
+        if is_truststore_enabled():
+            import truststore
+
+            truststore.inject_into_ssl()
+
 
 def main() -> int:
     exit_code: int = Application().run()
diff --git a/src/poetry/utils/ssl_truststore.py b/src/poetry/utils/ssl_truststore.py
new file mode 100644
index 00000000000..534fdae8e35
--- /dev/null
+++ b/src/poetry/utils/ssl_truststore.py
@@ -0,0 +1,32 @@
+from __future__ import annotations
+
+import logging
+import sys
+
+from poetry.config.config import Config
+
+
+logger = logging.getLogger(__name__)
+
+
+def _is_truststore_available() -> bool:
+    if sys.version_info < (3, 10):
+        logger.debug("Disabling truststore because Python version isn't 3.10+")
+        return False
+
+    try:
+        import ssl  # noqa: F401
+    except ImportError:
+        logger.warning("Disabling truststore since ssl support is missing")
+        return False
+
+    try:
+        import truststore  # noqa: F401
+    except ImportError:
+        logger.warning("Disabling truststore because `truststore` package is missing`")
+        return False
+    return True
+
+
+def is_truststore_enabled() -> bool:
+    return Config.create().get("system-truststore") and _is_truststore_available()
diff --git a/tests/conftest.py b/tests/conftest.py
index 39d71e172fc..931c83769b1 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -337,7 +337,8 @@ def git_mock(mocker: MockerFixture, request: FixtureRequest) -> None:
 
 
 @pytest.fixture
-def http() -> Iterator[type[httpretty.httpretty]]:
+def http(mocker: MockerFixture) -> Iterator[type[httpretty.httpretty]]:
+    mocker.patch("truststore.inject_into_ssl")
     httpretty.reset()
     with httpretty.enabled(allow_net_connect=False, verbose=True):
         yield httpretty
diff --git a/tests/console/commands/test_config.py b/tests/console/commands/test_config.py
index a6585c29145..9a709c47b91 100644
--- a/tests/console/commands/test_config.py
+++ b/tests/console/commands/test_config.py
@@ -64,6 +64,7 @@ def test_list_displays_default_value_if_not_set(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = true
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false
@@ -96,6 +97,7 @@ def test_list_displays_set_get_setting(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = false
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false
@@ -149,6 +151,7 @@ def test_unset_setting(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = true
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false
@@ -180,6 +183,7 @@ def test_unset_repo_setting(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = true
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false
@@ -309,6 +313,7 @@ def test_list_displays_set_get_local_setting(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = false
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false
@@ -349,6 +354,7 @@ def test_list_must_not_display_sources_from_pyproject_toml(
 requests.max-retries = 0
 solver.lazy-wheel = true
 system-git-client = false
+system-truststore = false
 virtualenvs.create = true
 virtualenvs.in-project = null
 virtualenvs.options.always-copy = false