diff --git a/pkg/sentry/fsimpl/proc/tasks_sys.go b/pkg/sentry/fsimpl/proc/tasks_sys.go
index dd57fdfdb..b2322a62d 100644
--- a/pkg/sentry/fsimpl/proc/tasks_sys.go
+++ b/pkg/sentry/fsimpl/proc/tasks_sys.go
@@ -20,6 +20,7 @@ import (
 	"math"
 
 	"gvisor.dev/gvisor/pkg/abi/linux"
+	"gvisor.dev/gvisor/pkg/atomicbitops"
 	"gvisor.dev/gvisor/pkg/context"
 	"gvisor.dev/gvisor/pkg/errors/linuxerr"
 	"gvisor.dev/gvisor/pkg/hostarch"
@@ -58,6 +59,9 @@ func (fs *filesystem) newSysDir(ctx context.Context, root *auth.Credentials, k *
 				"ptrace_scope": fs.newYAMAPtraceScopeFile(ctx, k, root),
 			}),
 		}),
+		"fs": fs.newStaticDir(ctx, root, map[string]kernfs.Inode{
+			"nr_open": fs.newInode(ctx, root, 0644, &atomicInt32File{val: &k.MaxFDLimit, min: 8, max: kernel.MaxFdLimit}),
+		}),
 		"vm": fs.newStaticDir(ctx, root, map[string]kernfs.Inode{
 			"max_map_count":     fs.newInode(ctx, root, 0444, newStaticFile("2147483647\n")),
 			"mmap_min_addr":     fs.newInode(ctx, root, 0444, &mmapMinAddrData{k: k}),
@@ -486,3 +490,49 @@ func (pr *portRange) Write(ctx context.Context, _ *vfs.FileDescription, src user
 	*pr.end = uint16(ports[1])
 	return n, nil
 }
+
+// atomicInt32File implements vfs.WritableDynamicBytesSource sysctls
+// represented by int32 atomic objects.
+//
+// +stateify savable
+type atomicInt32File struct {
+	kernfs.DynamicBytesFile
+
+	val      *atomicbitops.Int32
+	min, max int32
+}
+
+var _ vfs.WritableDynamicBytesSource = (*atomicInt32File)(nil)
+
+// Generate implements vfs.DynamicBytesSource.Generate.
+func (f *atomicInt32File) Generate(ctx context.Context, buf *bytes.Buffer) error {
+	_, err := fmt.Fprintf(buf, "%d\n", f.val.Load())
+	return err
+}
+
+// Write implements vfs.WritableDynamicBytesSource.Write.
+func (f *atomicInt32File) Write(ctx context.Context, _ *vfs.FileDescription, src usermem.IOSequence, offset int64) (int64, error) {
+	if offset != 0 {
+		// Ignore partial writes.
+		return 0, linuxerr.EINVAL
+	}
+	if src.NumBytes() == 0 {
+		return 0, nil
+	}
+
+	// Limit the amount of memory allocated.
+	src = src.TakeFirst(hostarch.PageSize - 1)
+
+	var v int32
+	n, err := usermem.CopyInt32StringInVec(ctx, src.IO, src.Addrs, &v, src.Opts)
+	if err != nil {
+		return 0, err
+	}
+
+	if v < f.min || v > f.max {
+		return 0, linuxerr.EINVAL
+	}
+
+	f.val.Store(v)
+	return n, nil
+}
diff --git a/pkg/sentry/kernel/fd_table.go b/pkg/sentry/kernel/fd_table.go
index 0ac275fb4..872eef160 100644
--- a/pkg/sentry/kernel/fd_table.go
+++ b/pkg/sentry/kernel/fd_table.go
@@ -231,18 +231,18 @@ func (f *FDTable) NewFDs(ctx context.Context, minFD int32, files []*vfs.FileDesc
 	}
 
 	// Default limit.
-	end := MaxFdLimit
+	end := f.k.MaxFDLimit.Load()
 
 	// Ensure we don't get past the provided limit.
 	if limitSet := limits.FromContext(ctx); limitSet != nil {
 		lim := limitSet.Get(limits.NumberOfFiles)
 		// Only set if the limit is smaller than the max to avoid overflow.
-		if lim.Cur != limits.Infinity && lim.Cur < uint64(MaxFdLimit) {
+		if lim.Cur != limits.Infinity && lim.Cur < uint64(end) {
 			end = int32(lim.Cur)
 		}
-		if minFD+int32(len(files)) > end {
-			return nil, unix.EMFILE
-		}
+	}
+	if minFD+int32(len(files)) > end {
+		return nil, unix.EMFILE
 	}
 
 	f.mu.Lock()
@@ -329,6 +329,9 @@ func (f *FDTable) newFDAt(ctx context.Context, fd int32, file *vfs.FileDescripti
 		return nil, unix.EBADF
 	}
 
+	if fd >= f.k.MaxFDLimit.Load() {
+		return nil, unix.EMFILE
+	}
 	// Check the limit for the provided file.
 	if limitSet := limits.FromContext(ctx); limitSet != nil {
 		if lim := limitSet.Get(limits.NumberOfFiles); lim.Cur != limits.Infinity && uint64(fd) >= lim.Cur {
diff --git a/pkg/sentry/kernel/fd_table_test.go b/pkg/sentry/kernel/fd_table_test.go
index 618070522..1ed7e8d31 100644
--- a/pkg/sentry/kernel/fd_table_test.go
+++ b/pkg/sentry/kernel/fd_table_test.go
@@ -69,6 +69,8 @@ func runTest(t testing.TB, fn func(ctx context.Context, fdTable *FDTable, fd *vf
 
 	// Create the table.
 	fdTable := new(FDTable)
+	fdTable.k = &Kernel{}
+	fdTable.k.MaxFDLimit.Store(MaxFdLimit)
 	fdTable.init()
 
 	// Run the test.
diff --git a/pkg/sentry/kernel/kernel.go b/pkg/sentry/kernel/kernel.go
index 0322c5a0e..b1c364ad6 100644
--- a/pkg/sentry/kernel/kernel.go
+++ b/pkg/sentry/kernel/kernel.go
@@ -323,6 +323,10 @@ type Kernel struct {
 	// userCountersMap maps auth.KUID into a set of user counters.
 	userCountersMap   map[auth.KUID]*UserCounters
 	userCountersMapMu userCountersMutex `state:"nosave"`
+
+	// MaxFDLimit specifies the maximum file descriptor number that can be
+	// used by processes.
+	MaxFDLimit atomicbitops.Int32
 }
 
 // InitKernelArgs holds arguments to Init.
@@ -367,6 +371,11 @@ type InitKernelArgs struct {
 
 	// PIDNamespace is the root PID namespace.
 	PIDNamespace *PIDNamespace
+
+	// MaxFDLimit specifies the maximum file descriptor number that can be
+	// used by processes.  If it is zero, the limit will be set to
+	// unlimited.
+	MaxFDLimit int32
 }
 
 // Init initialize the Kernel with no tasks.
@@ -420,6 +429,10 @@ func (k *Kernel) Init(args InitKernelArgs) error {
 	k.ptraceExceptions = make(map[*Task]*Task)
 	k.YAMAPtraceScope = atomicbitops.FromInt32(linux.YAMA_SCOPE_RELATIONAL)
 	k.userCountersMap = make(map[auth.KUID]*UserCounters)
+	if args.MaxFDLimit == 0 {
+		args.MaxFDLimit = MaxFdLimit
+	}
+	k.MaxFDLimit.Store(args.MaxFDLimit)
 
 	ctx := k.SupervisorContext()
 	if err := k.vfs.Init(ctx); err != nil {
diff --git a/pkg/sentry/syscalls/linux/sys_file.go b/pkg/sentry/syscalls/linux/sys_file.go
index 328f89196..ded2c8f50 100644
--- a/pkg/sentry/syscalls/linux/sys_file.go
+++ b/pkg/sentry/syscalls/linux/sys_file.go
@@ -565,6 +565,9 @@ func dup3(t *kernel.Task, oldfd, newfd int32, flags uint32) (uintptr, *kernel.Sy
 	err := t.NewFDAt(newfd, file, kernel.FDFlags{
 		CloseOnExec: flags&linux.O_CLOEXEC != 0,
 	})
+	if linuxerr.Equals(linuxerr.EMFILE, err) {
+		err = linuxerr.EBADF
+	}
 	if err != nil {
 		return 0, nil, err
 	}
diff --git a/pkg/sentry/syscalls/linux/sys_rlimit.go b/pkg/sentry/syscalls/linux/sys_rlimit.go
index 293a5c974..2995ba55e 100644
--- a/pkg/sentry/syscalls/linux/sys_rlimit.go
+++ b/pkg/sentry/syscalls/linux/sys_rlimit.go
@@ -108,6 +108,13 @@ func prlimit64(t *kernel.Task, resource limits.LimitType, newLim *limits.Limit)
 		return limits.Limit{}, linuxerr.EPERM
 	}
 
+	switch resource {
+	case limits.NumberOfFiles:
+		if newLim.Max > uint64(t.Kernel().MaxFDLimit.Load()) {
+			return limits.Limit{}, linuxerr.EPERM
+		}
+	}
+
 	// "A privileged process (under Linux: one with the CAP_SYS_RESOURCE
 	// capability in the initial user namespace) may make arbitrary changes
 	// to either limit value."
diff --git a/runsc/boot/loader.go b/runsc/boot/loader.go
index e680b02d5..fe8c45ec1 100644
--- a/runsc/boot/loader.go
+++ b/runsc/boot/loader.go
@@ -21,6 +21,7 @@ import (
 	mrand "math/rand"
 	"os"
 	"runtime"
+	"strconv"
 	gtime "time"
 
 	specs "github.com/opencontainers/runtime-spec/specs-go"
@@ -446,6 +447,19 @@ func New(args Args) (*Loader, error) {
 		log.Infof("Setting total memory to %.2f GB", float64(args.TotalMem)/(1<<30))
 	}
 
+	maxFDLimit := kernel.MaxFdLimit
+	if args.Spec.Linux != nil && args.Spec.Linux.Sysctl != nil {
+		if val, ok := args.Spec.Linux.Sysctl["fs.nr_open"]; ok {
+			nrOpen, err := strconv.Atoi(val)
+			if err != nil {
+				return nil, fmt.Errorf("setting fs.nr_open=%s: %w", val, err)
+			}
+			if nrOpen <= 0 || nrOpen > int(kernel.MaxFdLimit) {
+				return nil, fmt.Errorf("setting fs.nr_open=%s", val)
+			}
+			maxFDLimit = int32(nrOpen)
+		}
+	}
 	// Initiate the Kernel object, which is required by the Context passed
 	// to createVFS in order to mount (among other things) procfs.
 	if err = k.Init(kernel.InitKernelArgs{
@@ -458,6 +472,7 @@ func New(args Args) (*Loader, error) {
 		RootUTSNamespace:     kernel.NewUTSNamespace(args.Spec.Hostname, args.Spec.Hostname, creds.UserNamespace),
 		RootIPCNamespace:     kernel.NewIPCNamespace(creds.UserNamespace),
 		PIDNamespace:         kernel.NewRootPIDNamespace(creds.UserNamespace),
+		MaxFDLimit:           maxFDLimit,
 	}); err != nil {
 		return nil, fmt.Errorf("initializing kernel: %w", err)
 	}
diff --git a/test/syscalls/linux/BUILD b/test/syscalls/linux/BUILD
index 3012952aa..71540490e 100644
--- a/test/syscalls/linux/BUILD
+++ b/test/syscalls/linux/BUILD
@@ -621,7 +621,9 @@ cc_binary(
         "//test/util:eventfd_util",
         "//test/util:file_descriptor",
         "@com_google_absl//absl/memory",
+        "@com_google_absl//absl/strings",
         gtest,
+        "//test/util:capability_util",
         "//test/util:fs_util",
         "//test/util:posix_error",
         "//test/util:temp_path",
diff --git a/test/syscalls/linux/dup.cc b/test/syscalls/linux/dup.cc
index e1a74b5f9..a233f82b3 100644
--- a/test/syscalls/linux/dup.cc
+++ b/test/syscalls/linux/dup.cc
@@ -16,13 +16,16 @@
 #include <sys/resource.h>
 #include <unistd.h>
 
+#include <cerrno>
 #include <memory>
 
 #include "gtest/gtest.h"
 #include "absl/memory/memory.h"
+#include "absl/strings/str_cat.h"
 #include "test/util/eventfd_util.h"
 #include "test/util/file_descriptor.h"
 #include "test/util/fs_util.h"
+#include "test/util/linux_capability_util.h"
 #include "test/util/posix_error.h"
 #include "test/util/temp_path.h"
 #include "test/util/test_util.h"
@@ -140,6 +143,29 @@ TEST(DupTest, Rlimit) {
   EXPECT_EQ(fds.size() + used_fds, kFDLimit - fd.get() - 1);
 }
 
+TEST(RlimitTest, DupLimitedByNROpenSysctl) {
+  SKIP_IF(!ASSERT_NO_ERRNO_AND_VALUE(HaveCapability(CAP_SYS_RESOURCE)));
+
+  const int kNROpen = 1 << 22;
+  FileDescriptor fd =
+      ASSERT_NO_ERRNO_AND_VALUE(Open("/proc/sys/fs/nr_open", O_WRONLY));
+  auto data = absl::StrCat(kNROpen);
+  EXPECT_THAT(write(fd.get(), data.c_str(), data.size()),
+              SyscallSucceedsWithValue(data.size()));
+
+  struct rlimit rl = {
+      .rlim_cur = kNROpen + 1,
+      .rlim_max = kNROpen + 1,
+  };
+  EXPECT_THAT(setrlimit(RLIMIT_NOFILE, &rl), SyscallFailsWithErrno(EPERM));
+  rl.rlim_cur = kNROpen;
+  rl.rlim_max = kNROpen;
+  ASSERT_THAT(setrlimit(RLIMIT_NOFILE, &rl), SyscallSucceeds());
+
+  ASSERT_THAT(dup3(fd.get(), kNROpen, 0), SyscallFailsWithErrno(EBADF));
+  ASSERT_THAT(dup3(fd.get(), kNROpen - 1, 0), SyscallSucceeds());
+}
+
 TEST(DupTest, Dup2SameFD) {
   auto f = ASSERT_NO_ERRNO_AND_VALUE(TempPath::CreateFile());
   FileDescriptor fd = ASSERT_NO_ERRNO_AND_VALUE(Open(f.path(), O_RDONLY));