diff --git a/.pre-commit-config.yaml b/.pre-commit-config.yaml
index 27f360648..f3e50f595 100644
--- a/.pre-commit-config.yaml
+++ b/.pre-commit-config.yaml
@@ -63,7 +63,7 @@ repos:
         - '--options'
         - './girder/girder_large_image/web_client/package.json'
 - repo: https://github.com/asottile/pyupgrade
-  rev: v3.15.0
+  rev: v3.15.2
   hooks:
     - id: pyupgrade
       args:
@@ -71,7 +71,7 @@ repos:
         - --keep-percent-format
 - repo: https://github.com/astral-sh/ruff-pre-commit
   # Ruff version.
-  rev: v0.1.0
+  rev: v0.3.4
   hooks:
     - id: ruff
       args: [--fix, --exit-non-zero-on-fix]
@@ -81,11 +81,11 @@ repos:
   hooks:
     - id: autopep8
 - repo: https://github.com/PyCQA/flake8
-  rev: 6.1.0
+  rev: 7.0.0
   hooks:
     - id: flake8
 - repo: https://github.com/pycqa/isort
-  rev: 5.12.0
+  rev: 5.13.2
   hooks:
     - id: isort
       name: isort (python)
diff --git a/CHANGELOG.md b/CHANGELOG.md
index ed18b4e27..df9f04fcc 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -10,6 +10,7 @@
 - Add a dependency to the zarr source to read more compression types ([#1480](../../pull/1480))
 - Guard fetching internal metadata on zarr sources that have less data ([#1481](../../pull/1481))
 - Add a method to list registered extensions and mimetypes ([#1488](../../pull/1488))
+- Reduce bioformats keeping file handles open ([#1492](../../pull/1492))
 
 ### Changes
 - Prohibit bioformats from reading zip directly ([#1491](../../pull/1491))
diff --git a/pyproject.toml b/pyproject.toml
index 84bbde54b..f663fd7a5 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -9,7 +9,7 @@ exclude = [
     "*/web_client/*",
     "*/*egg*/*",
 ]
-ignore = [
+lint.ignore = [
     "B017",
     "B026",
     "B904",
@@ -38,7 +38,7 @@ ignore = [
     "PT017",
 ]
 line-length = 100
-select = [
+lint.select = [
     "B",  # bugbear
     "C90",  # mccabe
     "D",  # pydocstyle
@@ -61,14 +61,14 @@ select = [
     "RSE",
 ]
 
-[tool.ruff.per-file-ignores]
+[tool.ruff.lint.per-file-ignores]
 # allow "useless expressions" as it shows output
 # allow non-top level imports
 # allow long lines
 "docs/large_image_examples.ipynb" = ["B018", "E402", "E501"]
 
-[tool.ruff.flake8-quotes]
+[tool.ruff.lint.flake8-quotes]
 inline-quotes = "single"
 
-[tool.ruff.mccabe]
+[tool.ruff.lint.mccabe]
 max-complexity = 14
diff --git a/sources/bioformats/large_image_source_bioformats/__init__.py b/sources/bioformats/large_image_source_bioformats/__init__.py
index 71477572f..c04b6ac0f 100644
--- a/sources/bioformats/large_image_source_bioformats/__init__.py
+++ b/sources/bioformats/large_image_source_bioformats/__init__.py
@@ -221,7 +221,21 @@ def __init__(self, path, **kwargs):  # noqa
         try:
             javabridge.attach()
             try:
-                self._bioimage = bioformats.ImageReader(largeImagePath)
+                self._bioimage = bioformats.ImageReader(largeImagePath, perform_init=False)
+                try:
+                    # So this as a separate step so, if it fails, we can ask to
+                    # open something that does not exist and bioformats will
+                    # release some file handles.
+                    self._bioimage.init_reader()
+                except Exception as exc:
+                    try:
+                        # Ask to open a file that should never exist
+                        self._bioimage.rdr.setId('__\0__')
+                    except Exception:
+                        pass
+                    self._bioimage.close()
+                    self._bioimage = None
+                    raise exc
             except (AttributeError, OSError) as exc:
                 if not os.path.isfile(largeImagePath):
                     raise TileSourceFileNotFoundError(largeImagePath) from None
diff --git a/tox.ini b/tox.ini
index ef05e2848..20807ce05 100644
--- a/tox.ini
+++ b/tox.ini
@@ -172,7 +172,7 @@ deps =
   flake8-quotes
   ruff
 commands =
-  ruff large_image sources utilities girder girder_annotation examples docs test
+  ruff check large_image sources utilities girder girder_annotation examples docs test
   flake8
 
 [testenv:type]
@@ -213,7 +213,7 @@ skip_install = true
 deps =
   ruff
 commands =
-  ruff large_image sources utilities girder girder_annotation examples docs test {posargs}
+  ruff check large_image sources utilities girder girder_annotation examples docs test {posargs}
 
 [testenv:format]
 description = Autoformat import order and autopep8
@@ -228,7 +228,7 @@ commands =
   isort .
   autopep8 -ria large_image sources utilities girder girder_annotation examples docs test
   unify --in-place --recursive large_image sources utilities girder girder_annotation examples docs test
-  ruff large_image sources utilities girder girder_annotation examples docs test --fix
+  ruff check large_image sources utilities girder girder_annotation examples docs test --fix
 
 [testenv:lintclient]
 description = Lint the girder large_image plugin client