diff --git a/.ci/lint-python-bash.sh b/.ci/run-pre-commit-mypy.sh
similarity index 100%
rename from .ci/lint-python-bash.sh
rename to .ci/run-pre-commit-mypy.sh
diff --git a/.ci/test.sh b/.ci/test.sh
index 63da0e7d04a3..6b8f31135da9 100755
--- a/.ci/test.sh
+++ b/.ci/test.sh
@@ -115,7 +115,7 @@ if [[ $TASK == "lint" ]]; then
     # shellcheck disable=SC1091
     source activate "${CONDA_ENV}"
     echo "Linting Python and bash code"
-    bash ./.ci/lint-python-bash.sh || exit 1
+    bash ./.ci/run-pre-commit-mypy.sh || exit 1
     echo "Linting R code"
     Rscript ./.ci/lint-r-code.R "${BUILD_DIRECTORY}" || exit 1
     echo "Linting C++ code"
@@ -129,19 +129,8 @@ if [[ $TASK == "check-docs" ]] || [[ $TASK == "check-links" ]]; then
     conda env create \
         -n "${CONDA_ENV}" \
         --file ./docs/env.yml || exit 1
-    conda install \
-        -q \
-        -y \
-        -n "${CONDA_ENV}" \
-            'doxygen>=1.10.0' \
-            'rstcheck>=6.2.4' || exit 1
     # shellcheck disable=SC1091
     source activate "${CONDA_ENV}"
-    # check reStructuredText formatting
-    find "${BUILD_DIRECTORY}/python-package" -type f -name "*.rst" \
-        -exec rstcheck --report-level warning {} \+ || exit 1
-    find "${BUILD_DIRECTORY}/docs" -type f -name "*.rst" \
-        -exec rstcheck --report-level warning --ignore-directives=autoclass,autofunction,autosummary,doxygenfile {} \+ || exit 1
     # build docs
     make -C docs html || exit 1
     if [[ $TASK == "check-links" ]]; then
diff --git a/.pre-commit-config.yaml b/.pre-commit-config.yaml
index 9897937ab88a..6c8fc0f8335a 100644
--- a/.pre-commit-config.yaml
+++ b/.pre-commit-config.yaml
@@ -27,6 +27,15 @@ repos:
     hooks:
       - id: yamllint
         args: ["--strict"]
+  - repo: https://github.com/rstcheck/rstcheck
+    rev: v6.2.5
+    hooks:
+      - id: rstcheck
+        args: ["--config", "./python-package/pyproject.toml"]
+        additional_dependencies:
+          - breathe>=4.36.0
+          - sphinx>=8.1.3
+          - sphinx_rtd_theme>=3.0.1
   - repo: https://github.com/astral-sh/ruff-pre-commit
     # Ruff version.
     rev: v0.12.5
diff --git a/docs/env.yml b/docs/env.yml
index 30f84a26ce69..cf2bf82b247a 100644
--- a/docs/env.yml
+++ b/docs/env.yml
@@ -3,7 +3,8 @@ channels:
   - nodefaults
   - conda-forge
 dependencies:
-  - breathe>=4.35
+  - breathe>=4.36
+  - doxygen>=1.13.2
   - python=3.12
   - r-base>=4.3.3
   - r-data.table=1.16.4
diff --git a/python-package/README.rst b/python-package/README.rst
index 987269266488..ac20a4f56b79 100644
--- a/python-package/README.rst
+++ b/python-package/README.rst
@@ -346,7 +346,7 @@ To check that a contribution to the package matches its style expectations, run
 
 .. code:: sh
 
-    bash .ci/lint-python-bash.sh
+    bash .ci/run-pre-commit-mypy.sh
 
 To run the tests locally and compute test coverage, install the Python package using one of the options mentioned above.
 Then run the following from the root of the repo.
diff --git a/python-package/pyproject.toml b/python-package/pyproject.toml
index 088e031db9c8..b7ffd760ac94 100644
--- a/python-package/pyproject.toml
+++ b/python-package/pyproject.toml
@@ -91,6 +91,15 @@ disallow_untyped_defs = true
 exclude = 'build/*|compile/*|docs/*|examples/*|external_libs/*|lightgbm-python/*|tests/*'
 ignore_missing_imports = true
 
+[tool.rstcheck]
+report_level = "WARNING"
+ignore_directives = [
+    "autoclass",
+    "autofunction",
+    "autosummary",
+    "doxygenfile"
+]
+
 [tool.ruff]
 exclude = [
     "build",