diff --git a/.changelog/24125.txt b/.changelog/24125.txt
new file mode 100644
index 000000000000..a61ef2ea4f92
--- /dev/null
+++ b/.changelog/24125.txt
@@ -0,0 +1,3 @@
+```release-note:security
+security: Fixed a bug in client FS API where the check to prevent reads from the secrets dir could be bypassed on case-insensitive file systems
+```
diff --git a/.github/workflows/test-windows.yml b/.github/workflows/test-windows.yml
index f7d8f8d08b84..872d59e988b5 100644
--- a/.github/workflows/test-windows.yml
+++ b/.github/workflows/test-windows.yml
@@ -90,6 +90,7 @@ jobs:
             github.com/hashicorp/nomad/client/lib/fifo \
             github.com/hashicorp/nomad/client/logmon \
             github.com/hashicorp/nomad/client/allocrunner/taskrunner/template \
+            github.com/hashicorp/nomad/client/allocdir \
             github.com/hashicorp/nomad/plugins/base
       - uses: actions/upload-artifact@50769540e7f4bd5e21e526ee35c689e35e0d6874 # v4.4.0
         with:
diff --git a/client/allocdir/alloc_dir.go b/client/allocdir/alloc_dir.go
index 724e59da4542..65248460871a 100644
--- a/client/allocdir/alloc_dir.go
+++ b/client/allocdir/alloc_dir.go
@@ -471,11 +471,11 @@ func (d *AllocDir) ReadAt(path string, offset int64) (io.ReadCloser, error) {
 	// Check if it is trying to read into a secret directory
 	d.mu.RLock()
 	for _, dir := range d.TaskDirs {
-		if filepath.HasPrefix(p, dir.SecretsDir) {
+		if caseInsensitiveHasPrefix(p, dir.SecretsDir) {
 			d.mu.RUnlock()
 			return nil, fmt.Errorf("Reading secret file prohibited: %s", path)
 		}
-		if filepath.HasPrefix(p, dir.PrivateDir) {
+		if caseInsensitiveHasPrefix(p, dir.PrivateDir) {
 			d.mu.RUnlock()
 			return nil, fmt.Errorf("Reading private file prohibited: %s", path)
 		}
@@ -492,6 +492,11 @@ func (d *AllocDir) ReadAt(path string, offset int64) (io.ReadCloser, error) {
 	return f, nil
 }
 
+// CaseInsensitiveHasPrefix checks if the prefix is a case-insensitive prefix.
+func caseInsensitiveHasPrefix(s, prefix string) bool {
+	return strings.HasPrefix(strings.ToLower(s), strings.ToLower(prefix))
+}
+
 // BlockUntilExists blocks until the passed file relative the allocation
 // directory exists. The block can be cancelled with the passed context.
 func (d *AllocDir) BlockUntilExists(ctx context.Context, path string) (chan error, error) {
diff --git a/client/allocdir/alloc_dir_nonlinux_test.go b/client/allocdir/alloc_dir_nonlinux_test.go
new file mode 100644
index 000000000000..b1882e553294
--- /dev/null
+++ b/client/allocdir/alloc_dir_nonlinux_test.go
@@ -0,0 +1,60 @@
+// Copyright (c) HashiCorp, Inc.
+// SPDX-License-Identifier: BUSL-1.1
+
+//go:build !linux
+// +build !linux
+
+package allocdir
+
+import (
+	"os"
+	"path/filepath"
+	"testing"
+
+	"github.com/hashicorp/nomad/ci"
+	"github.com/hashicorp/nomad/helper/testlog"
+	"github.com/hashicorp/nomad/nomad/structs"
+	"github.com/hashicorp/nomad/plugins/drivers/fsisolation"
+	"github.com/shoenig/test/must"
+)
+
+func TestAllocDir_ReadAt_CaseInsensitiveSecretDir(t *testing.T) {
+	ci.Parallel(t)
+
+	// On macOS, os.TempDir returns a symlinked path under /var which
+	// is outside of the directories shared into the VM used for Docker.
+	// Expand the symlink to get the real path in /private, which is ok.
+	tmp, err := filepath.EvalSymlinks(t.TempDir())
+	must.NoError(t, err)
+
+	d := NewAllocDir(testlog.HCLogger(t), tmp, tmp, "test")
+	must.NoError(t, d.Build())
+	defer func() { _ = d.Destroy() }()
+
+	td := d.NewTaskDir(t1Windows)
+	must.NoError(t, td.Build(fsisolation.None, nil, "nobody"))
+
+	target := filepath.Join(t1Windows.Name, TaskSecrets, "test_file")
+
+	full := filepath.Join(d.AllocDir, target)
+	must.NoError(t, os.WriteFile(full, []byte("hi"), 0o600))
+
+	targetCaseInsensitive := filepath.Join(t1Windows.Name, "sEcReTs", "test_file")
+
+	_, err = d.ReadAt(targetCaseInsensitive, 0)
+	must.EqError(t, err, "Reading secret file prohibited: "+targetCaseInsensitive)
+}
+
+var (
+	t1Windows = &structs.Task{
+		Name:   "web",
+		Driver: "exec",
+		Config: map[string]interface{}{
+			"command": "/bin/date",
+			"args":    "+%s",
+		},
+		Resources: &structs.Resources{
+			DiskMB: 1,
+		},
+	}
+)
diff --git a/client/allocdir/alloc_dir_test.go b/client/allocdir/alloc_dir_test.go
index 22f2e04d3249..69f9e699598a 100644
--- a/client/allocdir/alloc_dir_test.go
+++ b/client/allocdir/alloc_dir_test.go
@@ -1,6 +1,9 @@
 // Copyright (c) HashiCorp, Inc.
 // SPDX-License-Identifier: BUSL-1.1
 
+//go:build !windows
+// +build !windows
+
 package allocdir
 
 import (
diff --git a/client/allocdir/fs_linux_test.go b/client/allocdir/fs_linux_test.go
index 073849d003d4..c6e6387c9334 100644
--- a/client/allocdir/fs_linux_test.go
+++ b/client/allocdir/fs_linux_test.go
@@ -1,6 +1,9 @@
 // Copyright (c) HashiCorp, Inc.
 // SPDX-License-Identifier: BUSL-1.1
 
+//go:build !windows
+// +build !windows
+
 package allocdir
 
 import (
diff --git a/client/allocdir/task_dir_test.go b/client/allocdir/task_dir_test.go
index 592aab2e5a95..f965b70d67ee 100644
--- a/client/allocdir/task_dir_test.go
+++ b/client/allocdir/task_dir_test.go
@@ -1,6 +1,9 @@
 // Copyright (c) HashiCorp, Inc.
 // SPDX-License-Identifier: BUSL-1.1
 
+//go:build !windows
+// +build !windows
+
 package allocdir
 
 import (