diff --git a/runner/cmd/runner/main.go b/runner/cmd/runner/main.go
index fc48233c6..27c07292b 100644
--- a/runner/cmd/runner/main.go
+++ b/runner/cmd/runner/main.go
@@ -38,7 +38,7 @@ func start(tempDir string, homeDir string, httpPort int, sshPort int, logLevel i
 	log.DefaultEntry.Logger.SetOutput(io.MultiWriter(os.Stdout, defaultLogFile))
 	log.DefaultEntry.Logger.SetLevel(logrus.Level(logLevel))
 
-	server, err := api.NewServer(tempDir, homeDir, fmt.Sprintf(":%d", httpPort), sshPort, version)
+	server, err := api.NewServer(context.TODO(), tempDir, homeDir, fmt.Sprintf(":%d", httpPort), sshPort, version)
 	if err != nil {
 		return fmt.Errorf("create server: %w", err)
 	}
diff --git a/runner/internal/metrics/cgroups.go b/runner/internal/metrics/cgroups.go
new file mode 100644
index 000000000..9ce1e54fe
--- /dev/null
+++ b/runner/internal/metrics/cgroups.go
@@ -0,0 +1,107 @@
+package metrics
+
+import (
+	"bufio"
+	"context"
+	"errors"
+	"fmt"
+	"os"
+	"strings"
+
+	"github.com/dstackai/dstack/runner/internal/log"
+)
+
+func getProcessCgroupMountPoint(ctx context.Context, ProcPidMountsPath string) (string, error) {
+	// See proc_pid_mounts(5) for the ProcPidMountsPath file description
+	file, err := os.Open(ProcPidMountsPath)
+	if err != nil {
+		return "", fmt.Errorf("open mounts file: %w", err)
+	}
+	defer func() {
+		_ = file.Close()
+	}()
+
+	mountPoint := ""
+	hasCgroupV1 := false
+
+	scanner := bufio.NewScanner(file)
+	for scanner.Scan() {
+		line := scanner.Text()
+		// See fstab(5) for the format description
+		fields := strings.Fields(line)
+		if len(fields) != 6 {
+			log.Warning(ctx, "Unexpected number of fields in mounts file", "num", len(fields), "line", line)
+			continue
+		}
+		fsType := fields[2]
+		if fsType == "cgroup2" {
+			mountPoint = fields[1]
+			break
+		}
+		if fsType == "cgroup" {
+			hasCgroupV1 = true
+		}
+	}
+	if err := scanner.Err(); err != nil {
+		log.Warning(ctx, "Error while scanning mounts file", "err", err)
+	}
+
+	if mountPoint != "" {
+		return mountPoint, nil
+	}
+
+	if hasCgroupV1 {
+		return "", errors.New("only cgroup v1 mounts found")
+	}
+
+	return "", errors.New("no cgroup mounts found")
+}
+
+func getProcessCgroupPathname(ctx context.Context, procPidCgroupPath string) (string, error) {
+	// See cgroups(7) for the procPidCgroupPath file description
+	file, err := os.Open(procPidCgroupPath)
+	if err != nil {
+		return "", fmt.Errorf("open cgroup file: %w", err)
+	}
+	defer func() {
+		_ = file.Close()
+	}()
+
+	pathname := ""
+	hasCgroupV1 := false
+
+	scanner := bufio.NewScanner(file)
+	for scanner.Scan() {
+		line := scanner.Text()
+		// See cgroups(7) for the format description
+		fields := strings.Split(line, ":")
+		if len(fields) != 3 {
+			log.Warning(ctx, "Unexpected number of fields in cgroup file", "num", len(fields), "line", line)
+			continue
+		}
+		if fields[0] != "0" {
+			hasCgroupV1 = true
+			continue
+		}
+		if fields[1] != "" {
+			// Must be empty for v2
+			log.Warning(ctx, "Unexpected v2 entry in cgroup file", "num", "line", line)
+			continue
+		}
+		pathname = fields[2]
+		break
+	}
+	if err := scanner.Err(); err != nil {
+		log.Warning(ctx, "Error while scanning cgroup file", "err", err)
+	}
+
+	if pathname != "" {
+		return pathname, nil
+	}
+
+	if hasCgroupV1 {
+		return "", errors.New("only cgroup v1 pathnames found")
+	}
+
+	return "", errors.New("no cgroup pathname found")
+}
diff --git a/runner/internal/metrics/cgroups_test.go b/runner/internal/metrics/cgroups_test.go
new file mode 100644
index 000000000..3e6e0abca
--- /dev/null
+++ b/runner/internal/metrics/cgroups_test.go
@@ -0,0 +1,87 @@
+package metrics
+
+import (
+	"fmt"
+	"os"
+	"path"
+	"testing"
+
+	"github.com/stretchr/testify/require"
+)
+
+const (
+	cgroup2MountLine = "cgroup2 /sys/fs/cgroup cgroup2 rw,nosuid,nodev,noexec,relatime,nsdelegate,memory_recursiveprot 0 0"
+	cgroupMountLine  = "cgroup /sys/fs/cgroup/cpu,cpuacct cgroup rw,nosuid,nodev,noexec,relatime,cpu,cpuacct 0 0"
+	rootMountLine    = "/dev/nvme0n1p5 / ext4 rw,relatime 0 0"
+)
+
+func TestGetProcessCgroupMountPoint_ErrorNoCgroupMounts(t *testing.T) {
+	procPidMountsPath := createProcFile(t, "mounts", rootMountLine, "malformed line")
+
+	mountPoint, err := getProcessCgroupMountPoint(t.Context(), procPidMountsPath)
+
+	require.ErrorContains(t, err, "no cgroup mounts found")
+	require.Equal(t, "", mountPoint)
+}
+
+func TestGetProcessCgroupMountPoint_ErrorOnlyCgroupV1Mounts(t *testing.T) {
+	procPidMountsPath := createProcFile(t, "mounts", rootMountLine, cgroupMountLine)
+
+	mountPoint, err := getProcessCgroupMountPoint(t.Context(), procPidMountsPath)
+
+	require.ErrorContains(t, err, "only cgroup v1 mounts found")
+	require.Equal(t, "", mountPoint)
+}
+
+func TestGetProcessCgroupMountPoint_OK(t *testing.T) {
+	procPidMountsPath := createProcFile(t, "mounts", rootMountLine, cgroupMountLine, cgroup2MountLine)
+
+	mountPoint, err := getProcessCgroupMountPoint(t.Context(), procPidMountsPath)
+
+	require.NoError(t, err)
+	require.Equal(t, "/sys/fs/cgroup", mountPoint)
+}
+
+func TestGetProcessCgroupPathname_ErrorNoCgroup(t *testing.T) {
+	procPidCgroupPath := createProcFile(t, "cgroup", "malformed entry")
+
+	mountPoint, err := getProcessCgroupPathname(t.Context(), procPidCgroupPath)
+
+	require.ErrorContains(t, err, "no cgroup pathname found")
+	require.Equal(t, "", mountPoint)
+}
+
+func TestGetProcessCgroupPathname_ErrorOnlyCgroupV1(t *testing.T) {
+	procPidCgroupPath := createProcFile(t, "cgroup", "7:cpu,cpuacct:/user.slice")
+
+	pathname, err := getProcessCgroupPathname(t.Context(), procPidCgroupPath)
+
+	require.ErrorContains(t, err, "only cgroup v1 pathnames found")
+	require.Equal(t, "", pathname)
+}
+
+func TestGetProcessCgroupPathname_OK(t *testing.T) {
+	procPidCgroupPath := createProcFile(t, "cgroup", "7:cpu,cpuacct:/user.slice", "0::/user.slice/user-1000.slice/session-1.scope")
+
+	mountPoint, err := getProcessCgroupPathname(t.Context(), procPidCgroupPath)
+
+	require.NoError(t, err)
+	require.Equal(t, "/user.slice/user-1000.slice/session-1.scope", mountPoint)
+}
+
+func createProcFile(t *testing.T, name string, lines ...string) string {
+	t.Helper()
+	tmpDir := t.TempDir()
+	pth := path.Join(tmpDir, name)
+	file, err := os.OpenFile(pth, os.O_WRONLY|os.O_CREATE, 0o600)
+	require.NoError(t, err)
+	defer func() {
+		err := file.Close()
+		require.NoError(t, err)
+	}()
+	for _, line := range lines {
+		_, err := fmt.Fprintln(file, line)
+		require.NoError(t, err)
+	}
+	return pth
+}
diff --git a/runner/internal/metrics/metrics.go b/runner/internal/metrics/metrics.go
index 0a5c1a639..26acc2cdf 100644
--- a/runner/internal/metrics/metrics.go
+++ b/runner/internal/metrics/metrics.go
@@ -7,6 +7,7 @@ import (
 	"fmt"
 	"os"
 	"os/exec"
+	"path"
 	"strconv"
 	"strings"
 	"time"
@@ -17,33 +18,42 @@ import (
 )
 
 type MetricsCollector struct {
-	cgroupVersion int
-	gpuVendor     common.GpuVendor
+	cgroupMountPoint string
+	gpuVendor        common.GpuVendor
 }
 
-func NewMetricsCollector() (*MetricsCollector, error) {
-	cgroupVersion, err := getCgroupVersion()
+func NewMetricsCollector(ctx context.Context) (*MetricsCollector, error) {
+	// It's unlikely that cgroup mount point will change during container lifetime,
+	// so we detect it only once and reuse.
+	cgroupMountPoint, err := getProcessCgroupMountPoint(ctx, "/proc/self/mounts")
 	if err != nil {
-		return nil, err
+		return nil, fmt.Errorf("get cgroup mount point: %w", err)
 	}
 	gpuVendor := common.GetGpuVendor()
 	return &MetricsCollector{
-		cgroupVersion: cgroupVersion,
-		gpuVendor:     gpuVendor,
+		cgroupMountPoint: cgroupMountPoint,
+		gpuVendor:        gpuVendor,
 	}, nil
 }
 
 func (s *MetricsCollector) GetSystemMetrics(ctx context.Context) (*schemas.SystemMetrics, error) {
+	// It's possible to move a process from one control group to another (it's unlikely, but nonetheless),
+	// so we detect the current group each time.
+	cgroupPathname, err := getProcessCgroupPathname(ctx, "/proc/self/cgroup")
+	if err != nil {
+		return nil, fmt.Errorf("get cgroup pathname: %w", err)
+	}
+	cgroupPath := path.Join(s.cgroupMountPoint, cgroupPathname)
 	timestamp := time.Now()
-	cpuUsage, err := s.GetCPUUsageMicroseconds()
+	cpuUsage, err := s.GetCPUUsageMicroseconds(cgroupPath)
 	if err != nil {
 		return nil, err
 	}
-	memoryUsage, err := s.GetMemoryUsageBytes()
+	memoryUsage, err := s.GetMemoryUsageBytes(cgroupPath)
 	if err != nil {
 		return nil, err
 	}
-	memoryCache, err := s.GetMemoryCacheBytes()
+	memoryCache, err := s.GetMemoryCacheBytes(cgroupPath)
 	if err != nil {
 		return nil, err
 	}
@@ -61,28 +71,14 @@ func (s *MetricsCollector) GetSystemMetrics(ctx context.Context) (*schemas.Syste
 	}, nil
 }
 
-func (s *MetricsCollector) GetCPUUsageMicroseconds() (uint64, error) {
-	cgroupCPUUsagePath := "/sys/fs/cgroup/cpu.stat"
-	if s.cgroupVersion == 1 {
-		cgroupCPUUsagePath = "/sys/fs/cgroup/cpuacct/cpuacct.usage"
-	}
+func (s *MetricsCollector) GetCPUUsageMicroseconds(cgroupPath string) (uint64, error) {
+	cgroupCPUUsagePath := path.Join(cgroupPath, "cpu.stat")
 
 	data, err := os.ReadFile(cgroupCPUUsagePath)
 	if err != nil {
 		return 0, fmt.Errorf("could not read CPU usage: %w", err)
 	}
 
-	if s.cgroupVersion == 1 {
-		// cgroup v1 provides usage in nanoseconds
-		usageStr := strings.TrimSpace(string(data))
-		cpuUsage, err := strconv.ParseUint(usageStr, 10, 64)
-		if err != nil {
-			return 0, fmt.Errorf("could not parse CPU usage: %w", err)
-		}
-		// convert nanoseconds to microseconds
-		return cpuUsage / 1000, nil
-	}
-	// cgroup v2, we need to extract usage_usec from cpu.stat
 	lines := strings.Split(string(data), "\n")
 	for _, line := range lines {
 		if strings.HasPrefix(line, "usage_usec") {
@@ -100,11 +96,8 @@ func (s *MetricsCollector) GetCPUUsageMicroseconds() (uint64, error) {
 	return 0, fmt.Errorf("usage_usec not found in cpu.stat")
 }
 
-func (s *MetricsCollector) GetMemoryUsageBytes() (uint64, error) {
-	cgroupMemoryUsagePath := "/sys/fs/cgroup/memory.current"
-	if s.cgroupVersion == 1 {
-		cgroupMemoryUsagePath = "/sys/fs/cgroup/memory/memory.usage_in_bytes"
-	}
+func (s *MetricsCollector) GetMemoryUsageBytes(cgroupPath string) (uint64, error) {
+	cgroupMemoryUsagePath := path.Join(cgroupPath, "memory.current")
 
 	data, err := os.ReadFile(cgroupMemoryUsagePath)
 	if err != nil {
@@ -119,11 +112,8 @@ func (s *MetricsCollector) GetMemoryUsageBytes() (uint64, error) {
 	return usedMemory, nil
 }
 
-func (s *MetricsCollector) GetMemoryCacheBytes() (uint64, error) {
-	cgroupMemoryStatPath := "/sys/fs/cgroup/memory.stat"
-	if s.cgroupVersion == 1 {
-		cgroupMemoryStatPath = "/sys/fs/cgroup/memory/memory.stat"
-	}
+func (s *MetricsCollector) GetMemoryCacheBytes(cgroupPath string) (uint64, error) {
+	cgroupMemoryStatPath := path.Join(cgroupPath, "memory.stat")
 
 	statData, err := os.ReadFile(cgroupMemoryStatPath)
 	if err != nil {
@@ -132,8 +122,7 @@ func (s *MetricsCollector) GetMemoryCacheBytes() (uint64, error) {
 
 	lines := strings.Split(string(statData), "\n")
 	for _, line := range lines {
-		if (s.cgroupVersion == 1 && strings.HasPrefix(line, "total_inactive_file")) ||
-			(s.cgroupVersion == 2 && strings.HasPrefix(line, "inactive_file")) {
+		if strings.HasPrefix(line, "inactive_file") {
 			parts := strings.Fields(line)
 			if len(parts) != 2 {
 				return 0, fmt.Errorf("unexpected format in memory.stat")
@@ -255,23 +244,6 @@ func (s *MetricsCollector) GetIntelAcceleratorMetrics(ctx context.Context) ([]sc
 	return parseNVIDIASMILikeMetrics(out.String())
 }
 
-func getCgroupVersion() (int, error) {
-	data, err := os.ReadFile("/proc/self/mountinfo")
-	if err != nil {
-		return 0, fmt.Errorf("could not read /proc/self/mountinfo: %w", err)
-	}
-
-	for _, line := range strings.Split(string(data), "\n") {
-		if strings.Contains(line, "cgroup2") {
-			return 2, nil
-		} else if strings.Contains(line, "cgroup") {
-			return 1, nil
-		}
-	}
-
-	return 0, fmt.Errorf("could not determine cgroup version")
-}
-
 func parseNVIDIASMILikeMetrics(output string) ([]schemas.GPUMetrics, error) {
 	metrics := []schemas.GPUMetrics{}
 
diff --git a/runner/internal/metrics/metrics_test.go b/runner/internal/metrics/metrics_test.go
index d547e2e33..152f31c1b 100644
--- a/runner/internal/metrics/metrics_test.go
+++ b/runner/internal/metrics/metrics_test.go
@@ -12,7 +12,7 @@ func TestGetAMDGPUMetrics_OK(t *testing.T) {
 	if runtime.GOOS == "darwin" {
 		t.Skip("Skipping on macOS")
 	}
-	collector, err := NewMetricsCollector()
+	collector, err := NewMetricsCollector(t.Context())
 	assert.NoError(t, err)
 
 	cases := []struct {
@@ -46,7 +46,7 @@ func TestGetAMDGPUMetrics_ErrorGPUUtilNA(t *testing.T) {
 	if runtime.GOOS == "darwin" {
 		t.Skip("Skipping on macOS")
 	}
-	collector, err := NewMetricsCollector()
+	collector, err := NewMetricsCollector(t.Context())
 	assert.NoError(t, err)
 	metrics, err := collector.getAMDGPUMetrics("gpu,gfx,gfx_clock,vram_used,vram_total\n0,N/A,N/A,283,196300\n")
 	assert.ErrorContains(t, err, "GPU utilization is N/A")
diff --git a/runner/internal/runner/api/http.go b/runner/internal/runner/api/http.go
index ac13b5e5b..bbf416efb 100644
--- a/runner/internal/runner/api/http.go
+++ b/runner/internal/runner/api/http.go
@@ -16,7 +16,6 @@ import (
 	"github.com/dstackai/dstack/runner/internal/api"
 	"github.com/dstackai/dstack/runner/internal/executor"
 	"github.com/dstackai/dstack/runner/internal/log"
-	"github.com/dstackai/dstack/runner/internal/metrics"
 	"github.com/dstackai/dstack/runner/internal/schemas"
 )
 
@@ -28,11 +27,10 @@ func (s *Server) healthcheckGetHandler(w http.ResponseWriter, r *http.Request) (
 }
 
 func (s *Server) metricsGetHandler(w http.ResponseWriter, r *http.Request) (interface{}, error) {
-	metricsCollector, err := metrics.NewMetricsCollector()
-	if err != nil {
-		return nil, &api.Error{Status: http.StatusInternalServerError, Err: err}
+	if s.metricsCollector == nil {
+		return nil, &api.Error{Status: http.StatusNotFound, Msg: "Metrics collector is not available"}
 	}
-	metrics, err := metricsCollector.GetSystemMetrics(r.Context())
+	metrics, err := s.metricsCollector.GetSystemMetrics(r.Context())
 	if err != nil {
 		return nil, &api.Error{Status: http.StatusInternalServerError, Err: err}
 	}
diff --git a/runner/internal/runner/api/server.go b/runner/internal/runner/api/server.go
index be573cc66..9d98315b1 100644
--- a/runner/internal/runner/api/server.go
+++ b/runner/internal/runner/api/server.go
@@ -12,6 +12,7 @@ import (
 	"github.com/dstackai/dstack/runner/internal/api"
 	"github.com/dstackai/dstack/runner/internal/executor"
 	"github.com/dstackai/dstack/runner/internal/log"
+	"github.com/dstackai/dstack/runner/internal/metrics"
 )
 
 type Server struct {
@@ -29,15 +30,23 @@ type Server struct {
 	executor  executor.Executor
 	cancelRun context.CancelFunc
 
+	metricsCollector *metrics.MetricsCollector
+
 	version string
 }
 
-func NewServer(tempDir string, homeDir string, address string, sshPort int, version string) (*Server, error) {
+func NewServer(ctx context.Context, tempDir string, homeDir string, address string, sshPort int, version string) (*Server, error) {
 	r := api.NewRouter()
 	ex, err := executor.NewRunExecutor(tempDir, homeDir, sshPort)
 	if err != nil {
 		return nil, err
 	}
+
+	metricsCollector, err := metrics.NewMetricsCollector(ctx)
+	if err != nil {
+		log.Warning(ctx, "Metrics collector is not available", "err", err)
+	}
+
 	s := &Server{
 		srv: &http.Server{
 			Addr:    address,
@@ -55,6 +64,8 @@ func NewServer(tempDir string, homeDir string, address string, sshPort int, vers
 
 		executor: ex,
 
+		metricsCollector: metricsCollector,
+
 		version: version,
 	}
 	r.AddHandler("GET", "/api/healthcheck", s.healthcheckGetHandler)
diff --git a/src/dstack/_internal/server/background/tasks/process_metrics.py b/src/dstack/_internal/server/background/tasks/process_metrics.py
index d2197d422..ca2d25fe5 100644
--- a/src/dstack/_internal/server/background/tasks/process_metrics.py
+++ b/src/dstack/_internal/server/background/tasks/process_metrics.py
@@ -140,8 +140,12 @@ async def _collect_job_metrics(job_model: JobModel) -> Optional[JobMetricsPoint]
         return None
 
     if res is None:
-        logger.warning(
-            "Failed to collect job %s metrics. Runner version does not support metrics API.",
+        logger.debug(
+            (
+                "Failed to collect job %s metrics."
+                " Either runner version does not support metrics API"
+                " or metrics collector is not available."
+            ),
             job_model.job_name,
         )
         return None