diff --git a/pkg/api/handlers/libpod/containers_create.go b/pkg/api/handlers/libpod/containers_create.go
index 429f45f91f..480cc656eb 100644
--- a/pkg/api/handlers/libpod/containers_create.go
+++ b/pkg/api/handlers/libpod/containers_create.go
@@ -62,6 +62,7 @@ func CreateContainer(w http.ResponseWriter, r *http.Request) {
 		utils.InternalServerError(w, err)
 		return
 	}
+
 	rtSpec, spec, opts, err := generate.MakeContainer(r.Context(), runtime, &sg, false, nil)
 	if err != nil {
 		utils.InternalServerError(w, err)
diff --git a/pkg/specgen/generate/container_create.go b/pkg/specgen/generate/container_create.go
index d73abced7e..7cfdd62127 100644
--- a/pkg/specgen/generate/container_create.go
+++ b/pkg/specgen/generate/container_create.go
@@ -15,6 +15,7 @@ import (
 	"github.com/containers/podman/v4/libpod/define"
 	"github.com/containers/podman/v4/pkg/namespaces"
 	"github.com/containers/podman/v4/pkg/specgen"
+	"github.com/containers/podman/v4/pkg/specgenutil"
 	"github.com/containers/podman/v4/pkg/util"
 	spec "github.com/opencontainers/runtime-spec/specs-go"
 	"github.com/opencontainers/selinux/go-selinux/label"
@@ -30,6 +31,12 @@ func MakeContainer(ctx context.Context, rt *libpod.Runtime, s *specgen.SpecGener
 		return nil, nil, nil, err
 	}
 
+	rlimits, err := specgenutil.GenRlimits(rtc.Ulimits())
+	if err != nil {
+		return nil, nil, nil, err
+	}
+	s.Rlimits = append(rlimits, s.Rlimits...)
+
 	// If joining a pod, retrieve the pod for use, and its infra container
 	var pod *libpod.Pod
 	var infra *libpod.Container
diff --git a/pkg/specgenutil/specgen.go b/pkg/specgenutil/specgen.go
index 4bf889fec9..3240eb9449 100644
--- a/pkg/specgenutil/specgen.go
+++ b/pkg/specgenutil/specgen.go
@@ -233,6 +233,28 @@ func setNamespaces(s *specgen.SpecGenerator, c *entities.ContainerCreateOptions)
 	return nil
 }
 
+func GenRlimits(ulimits []string) ([]specs.POSIXRlimit, error) {
+	rlimits := make([]specs.POSIXRlimit, 0, len(ulimits))
+	// Rlimits/Ulimits
+	for _, u := range ulimits {
+		if u == "host" {
+			rlimits = nil
+			break
+		}
+		ul, err := units.ParseUlimit(u)
+		if err != nil {
+			return nil, fmt.Errorf("ulimit option %q requires name=SOFT:HARD, failed to be parsed: %w", u, err)
+		}
+		rl := specs.POSIXRlimit{
+			Type: ul.Name,
+			Hard: uint64(ul.Hard),
+			Soft: uint64(ul.Soft),
+		}
+		rlimits = append(rlimits, rl)
+	}
+	return rlimits, nil
+}
+
 func FillOutSpecGen(s *specgen.SpecGenerator, c *entities.ContainerCreateOptions, args []string) error {
 	rtc, err := config.Default()
 	if err != nil {
@@ -738,21 +760,9 @@ func FillOutSpecGen(s *specgen.SpecGenerator, c *entities.ContainerCreateOptions
 	// DeviceCgroupRules: c.StringSlice("device-cgroup-rule"),
 
 	// Rlimits/Ulimits
-	for _, u := range c.Ulimit {
-		if u == "host" {
-			s.Rlimits = nil
-			break
-		}
-		ul, err := units.ParseUlimit(u)
-		if err != nil {
-			return fmt.Errorf("ulimit option %q requires name=SOFT:HARD, failed to be parsed: %w", u, err)
-		}
-		rl := specs.POSIXRlimit{
-			Type: ul.Name,
-			Hard: uint64(ul.Hard),
-			Soft: uint64(ul.Soft),
-		}
-		s.Rlimits = append(s.Rlimits, rl)
+	s.Rlimits, err = GenRlimits(c.Ulimit)
+	if err != nil {
+		return err
 	}
 
 	logOpts := make(map[string]string)
diff --git a/test/e2e/containers_conf_test.go b/test/e2e/containers_conf_test.go
index 90c4c7b42f..cbb451a5a0 100644
--- a/test/e2e/containers_conf_test.go
+++ b/test/e2e/containers_conf_test.go
@@ -55,6 +55,19 @@ var _ = Describe("Verify podman containers.conf usage", func() {
 		session.WaitWithDefaultTimeout()
 		Expect(session).Should(Exit(0))
 		Expect(session.OutputToString()).To(ContainSubstring("2048"))
+
+		// Reset CONTAINERS_CONF to "/dev/null"
+		// Local should go back to defaults but remote should be set on server side
+		os.Setenv("CONTAINERS_CONF", "/dev/null")
+		session = podmanTest.Podman([]string{"run", "--rm", fedoraMinimal, "ulimit", "-n"})
+		session.WaitWithDefaultTimeout()
+		Expect(session).Should(Exit(0))
+		if IsRemote() {
+			Expect(session.OutputToString()).To(ContainSubstring("500"))
+		} else {
+			Expect(session.OutputToString()).To(Not(Equal("500")))
+		}
+
 	})
 
 	It("having additional env", func() {
diff --git a/test/system/030-run.bats b/test/system/030-run.bats
index 753ec012e1..2f30941bcc 100644
--- a/test/system/030-run.bats
+++ b/test/system/030-run.bats
@@ -1006,6 +1006,24 @@ EOF
     CONTAINERS_CONF="$containersconf" run_podman 1 run --rm --read-only-tmpfs=false $IMAGE touch /tmp/testro
 }
 
+@test "podman run ulimit from containers.conf" {
+    skip_if_remote "containers.conf has to be set on remote, only tested on E2E test"
+    containersconf=$PODMAN_TMPDIR/containers.conf
+    nofile1=$((RANDOM % 10000 + 5))
+    nofile2=$((RANDOM % 10000 + 5))
+    cat >$containersconf <<EOF
+[containers]
+default_ulimits = [
+  "nofile=${nofile1}:${nofile1}",
+]
+EOF
+
+    CONTAINERS_CONF="$containersconf" run_podman run --rm $IMAGE grep "Max open files" /proc/self/limits
+    assert "$output" =~ " ${nofile1}  * ${nofile1}  * files"
+    CONTAINERS_CONF="$containersconf" run_podman run --ulimit nofile=${nofile2}:${nofile2} --rm $IMAGE grep "Max open files" /proc/self/limits
+    assert "$output" =~ " ${nofile2}  * ${nofile2}  * files"
+}
+
 @test "podman run bad --name" {
     randomname=$(random_string 30)
     run_podman 125 create --name "$randomname/bad" $IMAGE