diff --git a/op-e2e/faultproofs/output_cannon_test.go b/op-e2e/faultproofs/output_cannon_test.go
index 9373a1ac9335..e26719e05a92 100644
--- a/op-e2e/faultproofs/output_cannon_test.go
+++ b/op-e2e/faultproofs/output_cannon_test.go
@@ -70,6 +70,35 @@ func TestOutputCannonGame(t *testing.T) {
 	game.WaitForGameStatus(ctx, disputegame.StatusChallengerWins)
 }
 
+func TestOutputCannon_ChallengeAllZeroClaim(t *testing.T) {
+	// The dishonest actor always posts claims with all zeros.
+	op_e2e.InitParallel(t, op_e2e.UsesCannon, op_e2e.UseExecutor(outputCannonTestExecutor))
+	ctx := context.Background()
+	sys, l1Client := startFaultDisputeSystem(t)
+	t.Cleanup(sys.Close)
+
+	disputeGameFactory := disputegame.NewFactoryHelper(t, ctx, sys)
+	game := disputeGameFactory.StartOutputCannonGame(ctx, "sequencer", 3, common.Hash{})
+	game.LogGameData(ctx)
+
+	claim := game.DisputeLastBlock(ctx)
+	game.StartChallenger(ctx, "sequencer", "Challenger", challenger.WithPrivKey(sys.Cfg.Secrets.Alice))
+
+	game.DefendClaim(ctx, claim, func(parent *disputegame.ClaimHelper) *disputegame.ClaimHelper {
+		if parent.IsBottomGameRoot(ctx) {
+			return parent.Attack(ctx, common.Hash{})
+		}
+		return parent.Defend(ctx, common.Hash{})
+	})
+
+	game.LogGameData(ctx)
+
+	sys.TimeTravelClock.AdvanceTime(game.GameDuration(ctx))
+	require.NoError(t, wait.ForNextBlock(ctx, l1Client))
+	game.WaitForGameStatus(ctx, disputegame.StatusChallengerWins)
+	game.LogGameData(ctx)
+}
+
 func TestOutputCannon_PublishCannonRootClaim(t *testing.T) {
 	op_e2e.InitParallel(t, op_e2e.UsesCannon, op_e2e.UseExecutor(outputCannonTestExecutor))
 	tests := []struct {
diff --git a/op-program/host/cmd/main_test.go b/op-program/host/cmd/main_test.go
index 081136af117b..38cf29e6a4b6 100644
--- a/op-program/host/cmd/main_test.go
+++ b/op-program/host/cmd/main_test.go
@@ -239,6 +239,16 @@ func TestL2Claim(t *testing.T) {
 	t.Run("Invalid", func(t *testing.T) {
 		verifyArgsInvalid(t, config.ErrInvalidL2Claim.Error(), replaceRequiredArg("--l2.claim", "something"))
 	})
+
+	t.Run("Allows all zero without prefix", func(t *testing.T) {
+		cfg := configForArgs(t, replaceRequiredArg("--l2.claim", "0000000000000000000000000000000000000000000000000000000000000000"))
+		require.EqualValues(t, common.Hash{}, cfg.L2Claim)
+	})
+
+	t.Run("Allows all zero with prefix", func(t *testing.T) {
+		cfg := configForArgs(t, replaceRequiredArg("--l2.claim", "0x0000000000000000000000000000000000000000000000000000000000000000"))
+		require.EqualValues(t, common.Hash{}, cfg.L2Claim)
+	})
 }
 
 func TestL2BlockNumber(t *testing.T) {
diff --git a/op-program/host/config/config.go b/op-program/host/config/config.go
index 84d7c2e32908..117cdeadc9fd 100644
--- a/op-program/host/config/config.go
+++ b/op-program/host/config/config.go
@@ -85,9 +85,6 @@ func (c *Config) Check() error {
 	if c.L2OutputRoot == (common.Hash{}) {
 		return ErrInvalidL2OutputRoot
 	}
-	if c.L2Claim == (common.Hash{}) {
-		return ErrInvalidL2Claim
-	}
 	if c.L2ClaimBlockNumber == 0 {
 		return ErrInvalidL2ClaimBlock
 	}
@@ -151,9 +148,13 @@ func NewConfigFromCLI(log log.Logger, ctx *cli.Context) (*Config, error) {
 	if l2OutputRoot == (common.Hash{}) {
 		return nil, ErrInvalidL2OutputRoot
 	}
-	l2Claim := common.HexToHash(ctx.String(flags.L2Claim.Name))
-	if l2Claim == (common.Hash{}) {
-		return nil, ErrInvalidL2Claim
+	strClaim := ctx.String(flags.L2Claim.Name)
+	l2Claim := common.HexToHash(strClaim)
+	// Require a valid hash, with the zero hash explicitly allowed.
+	if l2Claim == (common.Hash{}) &&
+		strClaim != "0x0000000000000000000000000000000000000000000000000000000000000000" &&
+		strClaim != "0000000000000000000000000000000000000000000000000000000000000000" {
+		return nil, fmt.Errorf("%w: %v", ErrInvalidL2Claim, strClaim)
 	}
 	l2ClaimBlockNum := ctx.Uint64(flags.L2BlockNumber.Name)
 	l1Head := common.HexToHash(ctx.String(flags.L1Head.Name))
diff --git a/op-program/host/config/config_test.go b/op-program/host/config/config_test.go
index 13f7cdcb657f..2b85da110778 100644
--- a/op-program/host/config/config_test.go
+++ b/op-program/host/config/config_test.go
@@ -65,11 +65,11 @@ func TestL2OutputRootRequired(t *testing.T) {
 	require.ErrorIs(t, err, ErrInvalidL2OutputRoot)
 }
 
-func TestL2ClaimRequired(t *testing.T) {
+// The L2 claim may be provided by a dishonest actor so we must treat 0x00...00 as a real value.
+func TestL2ClaimMayBeDefaultValue(t *testing.T) {
 	config := validConfig()
 	config.L2Claim = common.Hash{}
-	err := config.Check()
-	require.ErrorIs(t, err, ErrInvalidL2Claim)
+	require.NoError(t, config.Check())
 }
 
 func TestL2ClaimBlockNumberRequired(t *testing.T) {