diff --git a/packages/api/internal/handlers/proxy_grpc.go b/packages/api/internal/handlers/proxy_grpc.go
index 7669ca1610..586a6824c6 100644
--- a/packages/api/internal/handlers/proxy_grpc.go
+++ b/packages/api/internal/handlers/proxy_grpc.go
@@ -18,6 +18,7 @@ import (
 	"github.com/e2b-dev/infra/packages/api/internal/utils"
 	dbtypes "github.com/e2b-dev/infra/packages/db/pkg/types"
 	"github.com/e2b-dev/infra/packages/shared/pkg/consts"
+	featureflags "github.com/e2b-dev/infra/packages/shared/pkg/feature-flags"
 	proxygrpc "github.com/e2b-dev/infra/packages/shared/pkg/grpc/proxy"
 	"github.com/e2b-dev/infra/packages/shared/pkg/logger"
 	sharedutils "github.com/e2b-dev/infra/packages/shared/pkg/utils"
@@ -98,10 +99,6 @@ func (s *SandboxService) ResumeSandbox(ctx context.Context, req *proxygrpc.Sandb
 
 	teamID := snap.Snapshot.TeamID
 
-	// Fixed 5 minutes for client-proxy initiated resume.
-	// This intentionally does not allow callers to override timeouts via gRPC.
-	timeout := 300 * time.Second
-
 	var autoResume *dbtypes.SandboxAutoResumeConfig
 	if snap.Snapshot.Config != nil {
 		autoResume = snap.Snapshot.Config.AutoResume
@@ -114,6 +111,8 @@ func (s *SandboxService) ResumeSandbox(ctx context.Context, req *proxygrpc.Sandb
 	if err != nil {
 		return nil, status.Errorf(codes.Internal, "failed to get team: %v", err)
 	}
+	minAutoResumeTimeout := time.Duration(s.api.featureFlags.IntFlag(ctx, featureflags.MinAutoResumeTimeoutSeconds)) * time.Second
+	timeout := calculateAutoResumeTimeout(autoResume, minAutoResumeTimeout, team)
 
 	autoPause := snap.Snapshot.AutoPause
 	nodeID := &snap.Snapshot.OriginNodeID
diff --git a/packages/api/internal/handlers/sandbox_create.go b/packages/api/internal/handlers/sandbox_create.go
index 31144aca11..6291332afc 100644
--- a/packages/api/internal/handlers/sandbox_create.go
+++ b/packages/api/internal/handlers/sandbox_create.go
@@ -144,6 +144,10 @@ func (a *APIStore) PostSandboxes(c *gin.Context) {
 
 		return
 	}
+	if autoResume != nil {
+		minAutoResumeTimeout := time.Duration(a.featureFlags.IntFlag(ctx, featureflags.MinAutoResumeTimeoutSeconds)) * time.Second
+		autoResume.Timeout = calculateTimeoutSeconds(timeout, minAutoResumeTimeout, teamInfo)
+	}
 
 	var envdAccessToken *string = nil
 	if body.Secure != nil && *body.Secure == true {
diff --git a/packages/api/internal/handlers/timeout_helper.go b/packages/api/internal/handlers/timeout_helper.go
new file mode 100644
index 0000000000..0d3a06eee1
--- /dev/null
+++ b/packages/api/internal/handlers/timeout_helper.go
@@ -0,0 +1,45 @@
+package handlers
+
+import (
+	"time"
+
+	typesteam "github.com/e2b-dev/infra/packages/auth/pkg/types"
+	dbtypes "github.com/e2b-dev/infra/packages/db/pkg/types"
+)
+
+const (
+	defaultProxyAutoResumeTimeout = 5 * time.Minute
+)
+
+func getTeamPlanLimit(team *typesteam.Team) time.Duration {
+	if team == nil || team.Limits == nil {
+		return 0
+	}
+
+	return time.Duration(team.Limits.MaxLengthHours) * time.Hour
+}
+
+func clampAutoResumeTimeout(requestedTimeout, teamPlanLimit, minAutoResumeTimeout time.Duration) time.Duration {
+	timeout := requestedTimeout
+	if teamPlanLimit > 0 && timeout > teamPlanLimit {
+		timeout = teamPlanLimit
+	}
+	if timeout < minAutoResumeTimeout {
+		timeout = minAutoResumeTimeout
+	}
+
+	return timeout
+}
+
+func calculateTimeoutSeconds(requestedTimeout, minAutoResumeTimeout time.Duration, team *typesteam.Team) uint64 {
+	return uint64(clampAutoResumeTimeout(requestedTimeout, getTeamPlanLimit(team), minAutoResumeTimeout).Seconds())
+}
+
+func calculateAutoResumeTimeout(autoResume *dbtypes.SandboxAutoResumeConfig, minAutoResumeTimeout time.Duration, team *typesteam.Team) time.Duration {
+	timeout := defaultProxyAutoResumeTimeout
+	if autoResume != nil && autoResume.Timeout > 0 {
+		timeout = time.Duration(autoResume.Timeout) * time.Second
+	}
+
+	return clampAutoResumeTimeout(timeout, getTeamPlanLimit(team), minAutoResumeTimeout)
+}
diff --git a/packages/api/internal/handlers/timeout_helper_test.go b/packages/api/internal/handlers/timeout_helper_test.go
new file mode 100644
index 0000000000..463e9e3c4c
--- /dev/null
+++ b/packages/api/internal/handlers/timeout_helper_test.go
@@ -0,0 +1,67 @@
+package handlers
+
+import (
+	"testing"
+	"time"
+
+	"github.com/stretchr/testify/require"
+
+	typesteam "github.com/e2b-dev/infra/packages/auth/pkg/types"
+	dbtypes "github.com/e2b-dev/infra/packages/db/pkg/types"
+)
+
+func testTeamWithMaxLengthHours(hours int64) *typesteam.Team {
+	return &typesteam.Team{
+		Limits: &typesteam.TeamLimits{
+			MaxLengthHours: hours,
+		},
+	}
+}
+
+// TestCalculateTimeoutSeconds verifies create-time timeout handling:
+// no timeout -> do not persist, short timeout -> min floor, long timeout -> team cap.
+func TestCalculateTimeoutSeconds(t *testing.T) {
+	t.Parallel()
+	team := testTeamWithMaxLengthHours(1)
+	minTimeout := time.Minute
+
+	// Create without explicit timeout should floor to the anti-thrash minimum.
+	timeout := calculateTimeoutSeconds(0, minTimeout, team)
+	require.Equal(t, uint64(60), timeout)
+
+	// Very short requests are floored to the anti-thrash minimum.
+	timeout = calculateTimeoutSeconds(15*time.Second, minTimeout, team)
+	require.Equal(t, uint64(60), timeout)
+
+	// Very long requests are capped by the team's maximum sandbox length.
+	timeout = calculateTimeoutSeconds(2*time.Hour, minTimeout, team)
+	require.Equal(t, uint64(3600), timeout)
+}
+
+// TestCalculateAutoResumeTimeout verifies resume-time timeout handling:
+// default fallback, persisted timeout minimum floor, and team cap.
+func TestCalculateAutoResumeTimeout(t *testing.T) {
+	t.Parallel()
+	team := testTeamWithMaxLengthHours(1)
+	minTimeout := time.Minute
+
+	// Older snapshots without persisted value should use the proxy fallback timeout.
+	timeout := calculateAutoResumeTimeout(nil, minTimeout, team)
+	require.Equal(t, 5*time.Minute, timeout)
+
+	// Persisted values below minimum are floored to the anti-thrash minimum.
+	timeout = calculateAutoResumeTimeout(
+		&dbtypes.SandboxAutoResumeConfig{Timeout: 20},
+		minTimeout,
+		team,
+	)
+	require.Equal(t, time.Minute, timeout)
+
+	// Persisted values above plan limit are capped by the team limit.
+	timeout = calculateAutoResumeTimeout(
+		&dbtypes.SandboxAutoResumeConfig{Timeout: 7200},
+		minTimeout,
+		team,
+	)
+	require.Equal(t, time.Hour, timeout)
+}
diff --git a/packages/api/internal/orchestrator/create_instance.go b/packages/api/internal/orchestrator/create_instance.go
index d65ec4a36e..5ac166f21f 100644
--- a/packages/api/internal/orchestrator/create_instance.go
+++ b/packages/api/internal/orchestrator/create_instance.go
@@ -215,9 +215,9 @@ func (o *Orchestrator) CreateSandbox(
 
 	var orchAutoResume *orchestrator.SandboxAutoResumeConfig
 	if autoResume != nil {
-		policy := string(autoResume.Policy)
 		orchAutoResume = &orchestrator.SandboxAutoResumeConfig{
-			Policy: policy,
+			Policy:         string(autoResume.Policy),
+			TimeoutSeconds: autoResume.Timeout,
 		}
 	}
 
diff --git a/packages/api/internal/orchestrator/nodemanager/sandboxes.go b/packages/api/internal/orchestrator/nodemanager/sandboxes.go
index 6715732d28..3482a8d890 100644
--- a/packages/api/internal/orchestrator/nodemanager/sandboxes.go
+++ b/packages/api/internal/orchestrator/nodemanager/sandboxes.go
@@ -80,9 +80,10 @@ func (n *Node) GetSandboxes(ctx context.Context) ([]sandbox.Sandbox, error) {
 
 		var autoResume *types.SandboxAutoResumeConfig
 		if autoResumeCfg := config.GetAutoResume(); autoResumeCfg != nil {
-			p := autoResumeCfg.GetPolicy()
-			policy := types.SandboxAutoResumePolicy(p)
-			autoResume = &types.SandboxAutoResumeConfig{Policy: policy}
+			autoResume = &types.SandboxAutoResumeConfig{
+				Policy:  types.SandboxAutoResumePolicy(autoResumeCfg.GetPolicy()),
+				Timeout: autoResumeCfg.GetTimeoutSeconds(),
+			}
 		}
 
 		sandboxesInfo = append(
diff --git a/packages/db/pkg/types/types.go b/packages/db/pkg/types/types.go
index 6054b39e88..beb5ea12c1 100644
--- a/packages/db/pkg/types/types.go
+++ b/packages/db/pkg/types/types.go
@@ -44,7 +44,8 @@ const (
 )
 
 type SandboxAutoResumeConfig struct {
-	Policy SandboxAutoResumePolicy `json:"policy"`
+	Policy  SandboxAutoResumePolicy `json:"policy"`
+	Timeout uint64                  `json:"timeout,omitempty"`
 }
 
 type PausedSandboxConfig struct {
diff --git a/packages/orchestrator/orchestrator.proto b/packages/orchestrator/orchestrator.proto
index e7170584e3..5c8a534188 100644
--- a/packages/orchestrator/orchestrator.proto
+++ b/packages/orchestrator/orchestrator.proto
@@ -56,6 +56,8 @@ message SandboxConfig {
 message SandboxAutoResumeConfig {
   // Policy values are owned by the API layer today (e.g. "off", "any").
   string policy = 1;
+  // Timeout requested on initial sandbox create (seconds).
+  uint64 timeout_seconds = 2;
 }
 
 message SandboxVolumeMount {
diff --git a/packages/shared/pkg/feature-flags/flags.go b/packages/shared/pkg/feature-flags/flags.go
index eab3c28aeb..7421b4786e 100644
--- a/packages/shared/pkg/feature-flags/flags.go
+++ b/packages/shared/pkg/feature-flags/flags.go
@@ -162,6 +162,10 @@ var (
 
 	// BuildBaseRootfsSizeLimitMB is the maximum size of the base rootfs filesystem created from the OCI image, in MB.
 	BuildBaseRootfsSizeLimitMB = newIntFlag("build-base-rootfs-size-limit-mb", 25000)
+
+	// MinAutoResumeTimeoutSeconds is the minimum auto-resume timeout in seconds.
+	// This prevents thrashing from very short timeouts.
+	MinAutoResumeTimeoutSeconds = newIntFlag("minimum-autoresume-timeout", 60)
 )
 
 type StringFlag struct {
diff --git a/packages/shared/pkg/grpc/orchestrator/orchestrator.pb.go b/packages/shared/pkg/grpc/orchestrator/orchestrator.pb.go
index 9f55acae95..cd1086ceff 100644
--- a/packages/shared/pkg/grpc/orchestrator/orchestrator.pb.go
+++ b/packages/shared/pkg/grpc/orchestrator/orchestrator.pb.go
@@ -267,6 +267,8 @@ type SandboxAutoResumeConfig struct {
 
 	// Policy values are owned by the API layer today (e.g. "off", "any").
 	Policy string `protobuf:"bytes,1,opt,name=policy,proto3" json:"policy,omitempty"`
+	// Timeout requested on initial sandbox create (seconds).
+	TimeoutSeconds uint64 `protobuf:"varint,2,opt,name=timeout_seconds,json=timeoutSeconds,proto3" json:"timeout_seconds,omitempty"`
 }
 
 func (x *SandboxAutoResumeConfig) Reset() {
@@ -308,6 +310,13 @@ func (x *SandboxAutoResumeConfig) GetPolicy() string {
 	return ""
 }
 
+func (x *SandboxAutoResumeConfig) GetTimeoutSeconds() uint64 {
+	if x != nil {
+		return x.TimeoutSeconds
+	}
+	return 0
+}
+
 type SandboxVolumeMount struct {
 	state         protoimpl.MessageState
 	sizeCache     protoimpl.SizeCache
@@ -1424,171 +1433,174 @@ var file_orchestrator_proto_rawDesc = []byte{
 	0x18, 0x0a, 0x16, 0x5f, 0x61, 0x6c, 0x6c, 0x6f, 0x77, 0x5f, 0x69, 0x6e, 0x74, 0x65, 0x72, 0x6e,
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 }
 
 var (
diff --git a/tests/integration/internal/tests/proxies/auto_resume_test.go b/tests/integration/internal/tests/proxies/auto_resume_test.go
index 3e5fdbc5a9..c58d295fa0 100644
--- a/tests/integration/internal/tests/proxies/auto_resume_test.go
+++ b/tests/integration/internal/tests/proxies/auto_resume_test.go
@@ -117,6 +117,106 @@ func TestSandboxAutoResumeViaProxy(t *testing.T) {
 	require.Equal(t, api.Running, res.JSON200.State, "sandbox should be running after auto-resume")
 }
 
+func TestSandboxAutoResumeWithoutExplicitTimeoutUsesMinimumTimeout(t *testing.T) {
+	t.Parallel()
+
+	c := setup.GetAPIClient()
+	ctx := t.Context()
+
+	autoPause := true
+	autoResume := api.SandboxAutoResumeConfig{Policy: api.Any}
+
+	// Create sandbox without passing timeout so API default is used.
+	createResp, err := c.PostSandboxesWithResponse(ctx, api.NewSandbox{
+		TemplateID: setup.SandboxTemplateID,
+		AutoPause:  &autoPause,
+		AutoResume: &autoResume,
+	}, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.Equal(t, http.StatusCreated, createResp.StatusCode())
+	require.NotNil(t, createResp.JSON201)
+
+	sbx := createResp.JSON201
+	t.Cleanup(func() {
+		utils.TeardownSandbox(t, c, sbx.SandboxID)
+	})
+
+	envdClient := setup.GetEnvdClient(t, ctx)
+
+	// Run ls before pausing.
+	err = utils.ExecCommand(t, ctx, sbx, envdClient, "ls")
+	require.NoError(t, err)
+
+	// Pause the sandbox.
+	pauseResp, err := c.PostSandboxesSandboxIDPauseWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.Equal(t, http.StatusNoContent, pauseResp.StatusCode())
+
+	// Run ls again — this should trigger auto-resume.
+	err = utils.ExecCommand(t, ctx, sbx, envdClient, "ls")
+	require.NoError(t, err)
+
+	// Verify auto-resume applies a minimum timeout (~60s) instead of 15s API default.
+	res, err := c.GetSandboxesSandboxIDWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.NotNil(t, res.JSON200, "expected 200 response, got status %d", res.StatusCode())
+	require.Equal(t, api.Running, res.JSON200.State, "sandbox should be running after auto-resume")
+	resumedDuration := res.JSON200.EndAt.Sub(res.JSON200.StartedAt)
+	require.InDelta(t, 60, resumedDuration.Seconds(), 15, "expected resumed timeout near 60s minimum, got %s", resumedDuration)
+}
+
+func TestSandboxAutoResumeUsesInitialTimeoutNotUpdatedTimeout(t *testing.T) {
+	t.Parallel()
+
+	c := setup.GetAPIClient()
+	ctx := t.Context()
+
+	// Create sandbox with explicit starting timeout.
+	sbx := utils.SetupSandboxWithCleanup(t, c, utils.WithTimeout(120), utils.WithAutoPause(true), utils.WithAutoResume(api.Any))
+	envdClient := setup.GetEnvdClient(t, ctx)
+
+	// Capture initial end time and update current timeout to a larger value.
+	res, err := c.GetSandboxesSandboxIDWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.NotNil(t, res.JSON200, "expected 200 response, got status %d", res.StatusCode())
+	require.Equal(t, api.Running, res.JSON200.State)
+	initialEndAt := res.JSON200.EndAt
+
+	timeoutResp, err := c.PostSandboxesSandboxIDTimeoutWithResponse(ctx, sbx.SandboxID, api.PostSandboxesSandboxIDTimeoutJSONRequestBody{
+		Timeout: 300,
+	}, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.Equal(t, http.StatusNoContent, timeoutResp.StatusCode())
+
+	res, err = c.GetSandboxesSandboxIDWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.NotNil(t, res.JSON200, "expected 200 response, got status %d", res.StatusCode())
+	require.Equal(t, api.Running, res.JSON200.State)
+	require.True(t, res.JSON200.EndAt.After(initialEndAt), "endAt should move forward after timeout update")
+
+	// Run ls before pausing.
+	err = utils.ExecCommand(t, ctx, sbx, envdClient, "ls")
+	require.NoError(t, err)
+
+	// Pause the sandbox.
+	pauseResp, err := c.PostSandboxesSandboxIDPauseWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.Equal(t, http.StatusNoContent, pauseResp.StatusCode())
+
+	// Run ls again — this should trigger auto-resume.
+	err = utils.ExecCommand(t, ctx, sbx, envdClient, "ls")
+	require.NoError(t, err)
+
+	// Verify auto-resume uses original starting timeout (120s), not updated timeout (300s).
+	res, err = c.GetSandboxesSandboxIDWithResponse(ctx, sbx.SandboxID, setup.WithAPIKey())
+	require.NoError(t, err)
+	require.NotNil(t, res.JSON200, "expected 200 response, got status %d", res.StatusCode())
+	require.Equal(t, api.Running, res.JSON200.State, "sandbox should be running after auto-resume")
+	resumedDuration := res.JSON200.EndAt.Sub(res.JSON200.StartedAt)
+	require.InDelta(t, 120, resumedDuration.Seconds(), 30, "expected timeout ~120s (starting timeout), got %s", resumedDuration)
+	require.Less(t, resumedDuration.Seconds(), 220.0, "resumed timeout should not follow updated 300s timeout")
+}
+
 func TestSandboxNoAutoResumeWithoutFlag(t *testing.T) {
 	t.Parallel()