diff --git a/CHANGELOG.md b/CHANGELOG.md
index c57999c1..ce88d94f 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -7,6 +7,9 @@ releases are available on [PyPI](https://pypi.org/project/pytask) and
 
 ## Unreleased
 
+- {pull}`739` closes file descriptors for the capture manager between CLI runs and
+  disposes stale database engines to prevent hitting OS file descriptor limits in
+  large test runs.
 - {pull}`725` fixes the pickle node hash test by accounting for Python 3.14's
   default pickle protocol.
 - {pull}`726` adapts the interactive debugger integration to Python 3.14's
diff --git a/src/_pytask/capture.py b/src/_pytask/capture.py
index c4201b1f..8d947710 100644
--- a/src/_pytask/capture.py
+++ b/src/_pytask/capture.py
@@ -57,6 +57,7 @@
     from types import TracebackType
 
     from _pytask.node_protocols import PTask
+    from _pytask.session import Session
 
 
 @hookimpl
@@ -109,6 +110,14 @@ def pytask_post_parse(config: dict[str, Any]) -> None:
     capman.suspend()
 
 
+@hookimpl
+def pytask_unconfigure(session: Session) -> None:
+    """Stop capturing and release file descriptors."""
+    capman = session.config["pm"].get_plugin("capturemanager")
+    if isinstance(capman, CaptureManager):
+        capman.stop_capturing()
+
+
 # Copied from pytest with slightly modified docstrings.
 
 
diff --git a/src/_pytask/database_utils.py b/src/_pytask/database_utils.py
index 77be06c5..63810343 100644
--- a/src/_pytask/database_utils.py
+++ b/src/_pytask/database_utils.py
@@ -14,6 +14,8 @@
 from _pytask.dag_utils import node_and_neighbors
 
 if TYPE_CHECKING:
+    from sqlalchemy.engine import Engine
+
     from _pytask.node_protocols import PNode
     from _pytask.node_protocols import PTask
     from _pytask.session import Session
@@ -29,6 +31,7 @@
 
 
 DatabaseSession = sessionmaker()
+_ENGINE: Engine | None = None
 
 
 class BaseTable(DeclarativeBase):
@@ -47,9 +50,12 @@ class State(BaseTable):
 
 def create_database(url: str) -> None:
     """Create the database."""
-    engine = create_engine(url)
-    BaseTable.metadata.create_all(bind=engine)
-    DatabaseSession.configure(bind=engine)
+    global _ENGINE  # noqa: PLW0603
+    if _ENGINE is not None:
+        _ENGINE.dispose()
+    _ENGINE = create_engine(url)
+    BaseTable.metadata.create_all(bind=_ENGINE)
+    DatabaseSession.configure(bind=_ENGINE)
 
 
 def _create_or_update_state(first_key: str, second_key: str, hash_: str) -> None: