diff --git a/test/preflight/apps_v2_integration_test.go b/test/preflight/apps_v2_integration_test.go
index 1294bc6734..41883f7a01 100644
--- a/test/preflight/apps_v2_integration_test.go
+++ b/test/preflight/apps_v2_integration_test.go
@@ -444,12 +444,14 @@ func testDeployDetach(t *testing.T) {
 	f := testlib.NewTestEnvFromEnv(t)
 	appName := f.CreateRandomAppName()
 
-	f.Fly("launch --org %s --name %s --region %s --now --internal-port 80 --image nginx --auto-confirm", f.OrgSlug(), appName, f.PrimaryRegion())
+	// With auto-stop on, the proxy stops these idle machines and deploy
+	// leaves them stopped, so they would never reach "started".
+	f.Fly("launch --org %s --name %s --region %s --now --internal-port 80 --image nginx --auto-confirm --auto-stop off", f.OrgSlug(), appName, f.PrimaryRegion())
 
 	ml := f.MachinesList(appName)
 	require.GreaterOrEqual(f, len(ml), 1)
 	m := ml[0]
-	f.Fly("machine wait %s --state started --wait-timeout 15s", m.ID)
+	f.Fly("machine wait %s --state started --wait-timeout 60s", m.ID)
 
 	res := f.Fly("deploy --detach")
 	require.NotContains(f, res.StdOutString(), "started")
@@ -457,7 +459,7 @@ func testDeployDetach(t *testing.T) {
 	ml = f.MachinesList(appName)
 	require.GreaterOrEqual(f, len(ml), 1)
 	m = ml[0]
-	f.Fly("machine wait %s --state started --wait-timeout 15s", m.ID)
+	f.Fly("machine wait %s --state started --wait-timeout 60s", m.ID)
 
 	res = f.Fly("deploy")
 	require.Contains(f, res.StdOutString(), "started")
@@ -467,13 +469,15 @@ func testDeployDetachBatching(t *testing.T) {
 	f := testlib.NewTestEnvFromEnv(t)
 	appName := f.CreateRandomAppName()
 
-	f.Fly("launch --org %s --name %s --region %s --now --internal-port 80 --image nginx --auto-confirm", f.OrgSlug(), appName, f.PrimaryRegion())
+	// With auto-stop on, the proxy stops these idle machines and deploy
+	// leaves them stopped, so they would never reach "started".
+	f.Fly("launch --org %s --name %s --region %s --now --internal-port 80 --image nginx --auto-confirm --auto-stop off", f.OrgSlug(), appName, f.PrimaryRegion())
 	f.Fly("scale count 6 --yes")
 
 	ml := f.MachinesList(appName)
 	require.GreaterOrEqual(f, len(ml), 1)
 	m := ml[0]
-	f.Fly("machine wait %s --state started --wait-timeout 15s", m.ID)
+	f.Fly("machine wait %s --state started --wait-timeout 60s", m.ID)
 
 	res := f.Fly("deploy --detach")
 	require.NotContains(f, res.StdOutString(), "started", false)
@@ -481,7 +485,7 @@ func testDeployDetachBatching(t *testing.T) {
 	ml = f.MachinesList(appName)
 	require.GreaterOrEqual(f, len(ml), 1)
 	m = ml[0]
-	f.Fly("machine wait %s --state started --wait-timeout 15s", m.ID)
+	f.Fly("machine wait %s --state started --wait-timeout 60s", m.ID)
 
 	res = f.Fly("deploy")
 	require.Contains(f, res.StdOutString(), "started", false)
diff --git a/test/preflight/fly_deploy_test.go b/test/preflight/fly_deploy_test.go
index dda5219ac7..f2e8e99d92 100644
--- a/test/preflight/fly_deploy_test.go
+++ b/test/preflight/fly_deploy_test.go
@@ -400,7 +400,9 @@ func TestFlyDeploy_DeployMachinesCheck(t *testing.T) {
 	useShortLivedDeployToken(t, f)
 	deployRes := f.Fly("deploy --buildkit --remote-only")
 	output := deployRes.StdOutString()
-	require.Contains(f, output, "Test Machine")
+	// The "Test Machine <id>: <state>" summary is skipped once the test
+	// machine has been destroyed, so check for the success line instead.
+	require.Regexp(f, `Test machine \S+ completed successfully`, output)
 }
 
 func TestFlyDeploy_NoServiceDeployMachinesCheck(t *testing.T) {
@@ -420,7 +422,9 @@ func TestFlyDeploy_NoServiceDeployMachinesCheck(t *testing.T) {
 	useShortLivedDeployToken(t, f)
 	deployRes := f.Fly("deploy --buildkit --remote-only")
 	output := deployRes.StdOutString()
-	require.Contains(f, output, "Test Machine")
+	// The "Test Machine <id>: <state>" summary is skipped once the test
+	// machine has been destroyed, so check for the success line instead.
+	require.Regexp(f, `Test machine \S+ completed successfully`, output)
 }
 
 // TODO: This test times out after ~15 minutes in CI (hangs at deploy command)
diff --git a/test/preflight/fly_launch_test.go b/test/preflight/fly_launch_test.go
index 27d3e6a662..eeb41fa09c 100644
--- a/test/preflight/fly_launch_test.go
+++ b/test/preflight/fly_launch_test.go
@@ -308,12 +308,19 @@ func TestFlyLaunchWithBuildSecrets(t *testing.T) {
 RUN --mount=type=secret,id=secret1 cat /run/secrets/secret1 > /tmp/secrets.txt
 `)
 
-	f.Fly("launch --org %s --name %s --region %s --internal-port 80 --ha=false --now --build-secret secret1=SECRET1 --remote-only", f.OrgSlug(), appName, f.PrimaryRegion())
+	f.Fly("launch --org %s --name %s --region %s --internal-port 80 --ha=false --now --build-secret secret1=SECRET1 --remote-only --auto-stop off", f.OrgSlug(), appName, f.PrimaryRegion())
 
+	// The machine may not accept SSH connections right after launch, so a
+	// failed or hung attempt must be retried rather than failing the test.
 	require.EventuallyWithT(t, func(c *assert.CollectT) {
-		ssh := f.Fly("ssh console -C 'cat /tmp/secrets.txt'")
-		assert.Equal(c, "SECRET1", ssh.StdOut().String())
-	}, 10*time.Second, 1*time.Second)
+		// The first attempt may need to start the agent and open a WireGuard
+		// tunnel, so give each attempt room for that.
+		ssh := f.FlyBestEffort(time.Minute, "ssh console -C 'cat /tmp/secrets.txt'")
+		if !assert.Equal(c, 0, ssh.ExitCode(), "ssh console failed: %s", ssh.StdErrString()) {
+			return
+		}
+		assert.Equal(c, "SECRET1", ssh.StdOutString())
+	}, 3*time.Minute, 2*time.Second)
 }
 
 func TestFlyLaunchBasicNodeApp(t *testing.T) {
diff --git a/test/preflight/fly_wireguard_test.go b/test/preflight/fly_wireguard_test.go
index 1936cc250b..1731d0e3e4 100644
--- a/test/preflight/fly_wireguard_test.go
+++ b/test/preflight/fly_wireguard_test.go
@@ -50,11 +50,18 @@ CMD ["sleep", "infinity"]
 
 		// The backend is eventually consistent. The peer may not be immediately visible.
 		assert.EventuallyWithT(t, func(t *assert.CollectT) {
-			result := f.Fly("machine exec -a %s %s 'dig +short aaaa @fdaa::3 %s._peer.internal'", appName, machineID, peerName)
+			// A failed or hung exec must be retried rather than failing the test.
+			result := f.FlyBestEffort(30*time.Second, "machine exec -a %s %s 'dig +short aaaa @fdaa::3 %s._peer.internal'", appName, machineID, peerName)
+			if !assert.Equal(t, 0, result.ExitCode(), "machine exec failed: %s", result.StdErrString()) {
+				return
+			}
 			assert.Contains(t, result.StdOutString(), "fdaa:")
 
-			result = f.Fly("machine exec -a %s %s 'dig +noall +answer txt @fdaa::3 _peer.internal'", appName, machineID)
+			result = f.FlyBestEffort(30*time.Second, "machine exec -a %s %s 'dig +noall +answer txt @fdaa::3 _peer.internal'", appName, machineID)
+			if !assert.Equal(t, 0, result.ExitCode(), "machine exec failed: %s", result.StdErrString()) {
+				return
+			}
 			assert.Contains(t, cleanupDigOutput(result.StdOutString()), peerName)
-		}, 10*time.Second, time.Second)
+		}, 2*time.Minute, 2*time.Second)
 	})
 }
diff --git a/test/preflight/testlib/result.go b/test/preflight/testlib/result.go
index 64e5fbb445..d7303890f2 100644
--- a/test/preflight/testlib/result.go
+++ b/test/preflight/testlib/result.go
@@ -20,6 +20,7 @@ type FlyctlResult struct {
 	testIoStreams         *iostreams.IOStreams
 	stdIn, stdOut, stdErr *bytes.Buffer
 	exitCode              int
+	timedOut              bool
 }
 
 func (r *FlyctlResult) CmdString() string {
@@ -30,6 +31,11 @@ func (r *FlyctlResult) ExitCode() int {
 	return r.exitCode
 }
 
+// TimedOut reports whether the command was killed for exceeding its deadline.
+func (r *FlyctlResult) TimedOut() bool {
+	return r.timedOut
+}
+
 func (r *FlyctlResult) StdOut() *bytes.Buffer {
 	return r.stdOut
 }
diff --git a/test/preflight/testlib/test_env.go b/test/preflight/testlib/test_env.go
index a06e863139..31d43832fb 100644
--- a/test/preflight/testlib/test_env.go
+++ b/test/preflight/testlib/test_env.go
@@ -10,6 +10,7 @@ import (
 	"os/exec"
 	"path/filepath"
 	"strings"
+	"sync"
 	"testing"
 	"time"
 
@@ -30,10 +31,13 @@ type FlyctlTestEnv struct {
 	primaryRegion       string
 	otherRegions        []string
 	env                 map[string]string
-	cmdHistory          []*FlyctlResult
-	noHistoryOnFail     bool
-	id                  string
-	VMSize              string
+	// historyMu guards cmdHistory, which retry goroutines that outlive an
+	// EventuallyWithT call can still append to.
+	historyMu       sync.Mutex
+	cmdHistory      []*FlyctlResult
+	noHistoryOnFail bool
+	id              string
+	VMSize          string
 }
 
 // Preflight flyctl commands are not supposed to take more than five minutes.
@@ -213,8 +217,22 @@ func (f *FlyctlTestEnv) FlyAllowExitFailure(flyctlCmd string, vals ...interface{
 	return f.FlyContextAndConfig(ctx, FlyCmdConfig{NoAssertSuccessfulExit: true}, flyctlCmd, vals...)
 }
 
+// FlyBestEffort runs flyctl command with the given timeout and returns the result.
+// It does not fail the test because of the command's outcome: a non-zero exit
+// is reported by ExitCode, and a command that exceeds the timeout is killed and
+// reported by TimedOut. This makes it safe for retry loops and cleanup.
+func (f *FlyctlTestEnv) FlyBestEffort(timeout time.Duration, flyctlCmd string, vals ...interface{}) *FlyctlResult {
+	ctx, cancel := context.WithTimeout(context.Background(), timeout)
+	defer cancel()
+
+	return f.FlyContextAndConfig(ctx, FlyCmdConfig{NoAssertSuccessfulExit: true, NoAssertDeadline: true}, flyctlCmd, vals...)
+}
+
 type FlyCmdConfig struct {
 	NoAssertSuccessfulExit bool
+	// NoAssertDeadline reports a command that exceeds its context deadline
+	// through TimedOut instead of failing the test.
+	NoAssertDeadline bool
 }
 
 func (f *FlyctlTestEnv) FlyContextAndConfig(ctx context.Context, cfg FlyCmdConfig, flyctlCmd string, vals ...interface{}) *FlyctlResult {
@@ -253,16 +271,24 @@ func (f *FlyctlTestEnv) FlyContextAndConfig(ctx context.Context, cfg FlyCmdConfi
 	}
 	err = cmd.Wait()
 	if err != nil && ctx.Err() != nil {
-		f.Fatalf("command exceeded its deadline: %s [context error]: %v [stdout]: %s [stderr]: %s", res.cmdStr, ctx.Err(), res.stdOut.String(), res.stdErr.String())
-	}
-	if err == nil {
+		if !cfg.NoAssertDeadline {
+			f.Fatalf("command exceeded its deadline: %s [context error]: %v [stdout]: %s [stderr]: %s", res.cmdStr, ctx.Err(), res.stdOut.String(), res.stdErr.String())
+		}
+		// Record the timeout in stderr rather than logging it: this may run in a
+		// retry goroutine that outlives the test, where t.Logf panics.
+		fmt.Fprintf(res.stdErr, "\ncommand exceeded its deadline: %v", ctx.Err())
+		res.exitCode = -1
+		res.timedOut = true
+	} else if err == nil {
 		res.exitCode = 0
 	} else if exitErr, ok := err.(*exec.ExitError); ok {
 		res.exitCode = exitErr.ExitCode()
 	} else {
 		f.Fatalf("unexpected error waiting on command: %s [error]: %v", res.cmdStr, err)
 	}
+	f.historyMu.Lock()
 	f.cmdHistory = append(f.cmdHistory, res)
+	f.historyMu.Unlock()
 	if !cfg.NoAssertSuccessfulExit {
 		res.AssertSuccessfulExit()
 	}
@@ -282,7 +308,10 @@ func (f *FlyctlTestEnv) DebugPrintHistory() {
 	if f.Failed() || f.noHistoryOnFail {
 		return
 	}
-	for i, r := range f.cmdHistory {
+	f.historyMu.Lock()
+	history := append([]*FlyctlResult(nil), f.cmdHistory...)
+	f.historyMu.Unlock()
+	for i, r := range history {
 		fmt.Printf("%3d:\n", i+1)
 		r.DebugPrintOutput()
 	}
@@ -321,7 +350,12 @@ func (f *FlyctlTestEnv) CreateRandomAppName() string {
 
 	appName := randomName(f, prefix)
 	f.Cleanup(func() {
-		f.FlyAllowExitFailure("apps destroy --yes %s", appName)
+		// A slow destroy shouldn't fail a test that already passed, or hold up
+		// the suite. Apps left behind are removed by the preflight cleanup workflow.
+		res := f.FlyBestEffort(time.Minute, "apps destroy --yes %s", appName)
+		if res.ExitCode() != 0 {
+			f.Logf("apps destroy %s failed (timed out: %t); leaving it for the preflight cleanup workflow: %s", appName, res.TimedOut(), res.StdErrString())
+		}
 	})
 	return appName
 }