Objectives: To assess fetal circulating free fetal haemoglobin (fHbF) levels and heme defences, correlated to fetal circulatory biometry and fetal sex in severe early-onset fetal growth restriction. Design, Setting & Population: A prospective study severe early-onset fetal growth restriction pregnancies with close clinical management (EFW<3 ^rd centile and <600g at 20-26+6 weeks; N=20). Method & Main Outcome Measures: Temporal fetal vascular obstetric biometry was recorded. Cord blood fHbF and key heme-scavenger defences were measured and compared with normal term births (N=26) and births with late-onset FGR (N=12). Results: fHbF was elevated in early-onset FGR compared with normal pregnancy: 0.437(0.337/0.753) mg/mL; P<0.0001; 0.098(0.045/0.264) mg/mL; P<0.0001), respectively; whilst hemopexin was downregulated in early- and late-onset FGR compared to normal pregnancy: 36(14/81) μg/mL, P<0.001; 25(19/40) μg/mL, P<0.0001; 155(132/219) μg/mL, respectively; median(interquartile ranges). Early-onset FGR male fetuses had higher fetal haemoglobin compared with the normal males: 0.710(0.433/0.857) mg/mL; P<0.001; 0.099(0.043/0.246) mg/mL, respectively; median(interquartile ranges). In early-onset FGR, ratios of mid-cerebral artery and umbilical artery pulsatility indices correlated positively with heme-scavenger levels (hemopexin and a heme-handling composite measure: P<0.05 and P<0.01, respectively), indicating lower levels are associated with cerebral vascular redistribution. These heme handling measures also positively correlated with gestational age at delivery (P<0.01, both) and birthweight (P<0.001 and P<0.05, respectively). Conclusion: Free fetal haemoglobin overproduction may be one route to placental vascular compromise in early-onset FGR, implicated in reduced placental and fetal blood flow.