diff --git a/news/4079.fixed.md b/news/4079.fixed.md
new file mode 100644
index 0000000000..7e1c3237ae
--- /dev/null
+++ b/news/4079.fixed.md
@@ -0,0 +1,4 @@
+(toolchain) Fixed a crash in {obj}`py_test` main validation
+({obj}`validate_test_main`) on Windows: the interpreter used for the check
+couldn't find its DLLs or its stdlib once relocated
+([#4079](https://github.com/bazel-contrib/rules_python/issues/4079)).
diff --git a/python/private/py_executable.bzl b/python/private/py_executable.bzl
index 0e7e292aae..0e9c315a73 100644
--- a/python/private/py_executable.bzl
+++ b/python/private/py_executable.bzl
@@ -64,7 +64,6 @@ load(":py_cc_link_params_info.bzl", "PyCcLinkParamsInfo")
 load(":py_executable_info.bzl", "PyExecutableInfo")
 load(":py_info.bzl", "PyInfo", "VenvSymlinkKind")
 load(":py_internal.bzl", "py_internal")
-load(":py_interpreter_program.bzl", "PyInterpreterProgramInfo")
 load(":py_runtime_info.bzl", "DEFAULT_STUB_SHEBANG")
 load(":reexports.bzl", "BuiltinPyInfo", "BuiltinPyRuntimeInfo")
 load(":rule_builders.bzl", "ruleb")
@@ -1348,47 +1347,33 @@ def _maybe_add_test_main_validation(ctx, main_py, output_groups):
         return
 
     exec_tools_toolchain = ctx.toolchains[EXEC_TOOLS_TOOLCHAIN_TYPE]
-    if exec_tools_toolchain == None or exec_tools_toolchain.exec_tools.exec_interpreter == None:
+    if (
+        exec_tools_toolchain == None or
+        exec_tools_toolchain.exec_tools.exec_runtime == None
+    ):
         fail(
             "Validating py_test main modules requires the exec tools toolchain " +
-            "with an exec interpreter, but none was found. Either register one " +
+            "with an exec runtime, but none was found. Either register one " +
             "or set --@rules_python//python/config_settings:validate_test_main=disabled.",
         )
 
-    exec_tools = exec_tools_toolchain.exec_tools
     validator = ctx.attr._validate_test_main
-    program_info = validator[PyInterpreterProgramInfo]
-    interpreter = exec_tools.exec_interpreter[DefaultInfo].files_to_run
-    validator_files_to_run = validator[DefaultInfo].files_to_run
-
     validation_output = ctx.actions.declare_file(ctx.label.name + "_validate_test_main.txt")
 
     args = ctx.actions.args()
-    args.add_all(program_info.interpreter_args)
-    args.add(validator_files_to_run.executable)
     args.add("--src", main_py)
     args.add("--src_name", main_py.short_path)
     args.add("--label", str(ctx.label))
     args.add("--output", validation_output)
 
-    execution_requirements = {}
-    if testing.ExecutionInfo in validator:
-        execution_requirements = validator[testing.ExecutionInfo].requirements
-
-    ctx.actions.run(
-        executable = interpreter,
+    actions_run(
+        ctx,
+        executable = validator,
         arguments = [args],
         inputs = [main_py],
         outputs = [validation_output],
-        tools = [validator_files_to_run],
         mnemonic = "PyValidateTestMain",
         progress_message = "Validating py_test main %{label}",
-        env = program_info.env | {
-            "PYTHONNOUSERSITE": "1",
-            "PYTHONSAFEPATH": "1",
-        },
-        execution_requirements = execution_requirements,
-        toolchain = EXEC_TOOLS_TOOLCHAIN_TYPE,
     )
     if "_validation" in output_groups:
         output_groups["_validation"] = depset([validation_output], transitive = [output_groups["_validation"]])
diff --git a/tests/integration/BUILD.bazel b/tests/integration/BUILD.bazel
index 13b9c2e855..2eae8dfecb 100644
--- a/tests/integration/BUILD.bazel
+++ b/tests/integration/BUILD.bazel
@@ -52,6 +52,7 @@ test_suite(
         "bzlmod_lockfile_test_bazel_9.1.0",
         "local_toolchains_test_bazel_self",
         "uv_lock_test_bazel_self",
+        "validate_test_main_test_bazel_self",
     ],
 )
 
diff --git a/tests/integration/runner.py b/tests/integration/runner.py
index 9efcbebb89..23e41f6cf1 100644
--- a/tests/integration/runner.py
+++ b/tests/integration/runner.py
@@ -63,10 +63,10 @@ def describe(self) -> str:
 {env} \\
   {args}
 RESULT: exit_code: {self.exit_code}
-===== STDOUT START =====
-{self.stdout}{maybe_stdout_nl}===== STDOUT END   =====
-===== STDERR START =====
-{self.stderr}{maybe_stderr_nl}===== STDERR END   =====
+==================== STDOUT BEGIN ====================
+{self.stdout}{maybe_stdout_nl}==================== STDOUT END ====================
+==================== STDERR BEGIN ====================
+{self.stderr}{maybe_stderr_nl}==================== STDERR END ====================
 """
 
 
@@ -74,7 +74,17 @@ class TestCase(unittest.TestCase):
     def setUp(self):
         super().setUp()
         self.repo_root = pathlib.Path(os.environ["BIT_WORKSPACE_DIR"])
-        self.bazel = pathlib.Path(os.environ["BIT_BAZEL_BINARY"])
+        bazel = pathlib.Path(os.environ["BIT_BAZEL_BINARY"])
+        # Windows doesn't interpret shebangs, so prepend any script interpreter.
+        interpreter = []
+        if os.name == "nt":
+            with bazel.open("rb") as f:
+                first_line = f.readline()
+            if first_line.startswith(b"#!"):
+                interpreter = first_line[2:].decode().split()
+                if interpreter and interpreter[0].endswith("/env"):
+                    interpreter = interpreter[1:]
+        self.bazel_cmd = (*interpreter, str(bazel))
         outer_test_tmpdir = pathlib.Path(os.environ["TEST_TMPDIR"])
         self.test_tmp_dir = outer_test_tmpdir / "bit_test_tmp"
         # Put the global tmp not under the test tmp to better match how a real
@@ -103,7 +113,7 @@ def run_bazel(self, *args: str, check: bool = True) -> ExecuteResult:
         Returns:
             An `ExecuteResult` from running Bazel
         """
-        cmd_args = [str(self.bazel), *args]
+        cmd_args = [*self.bazel_cmd, *args]
         env = self.bazel_env
         _logger.info("executing: %s", shlex.join(cmd_args))
         cwd = self.repo_root