Placental malaria can lead to poor neonatal outcomes, including low birthweight due to fetal growth restriction, especially when associated with local inflammation (intervillositis). The pathogenesis of placental malaria-associated fetal growth restriction is largely unknown but, in idiopathic fetal growth restriction, impaired transplacental amino acid transport, especially through the system A group of amino acid transporters, has been implicated. We hypothesized that placental malaria-associated fetal growth restriction could result from impairment of transplacental amino acid transport triggered by intervillositis. In a cohort of Malawian women and their infants, the expression and activity of system A (measured by Na+-dependent 14C-MeAIB uptake) were reduced in placental malaria, especially when associated with intervillositis, compared to uninfected placentas. In an in vitro model of placental malaria with intervillositis, placental cells exposed to monocyte/infected erythrocytes conditioned medium showed decreased system A activity. Amino acid concentrations analyzed by reversed phase ultra performance liquid chromatography in paired maternal and cord plasmas revealed specific alterations of amino acid transport by placental malaria, especially with intervillositis. Overall, our data suggest that the fetoplacental unit responds to placental malaria by altering its placental amino acid transport to maintain adequate fetal growth. However, intervillositis more profoundly compromises placental amino acid transport function, leading to fetal growth restriction. Our study offers the first pathogenetic explanation for fetal growth restriction in placental malaria.