Elucidation of the evolutionary history and interrelatedness ofPlasmodiumspecies that infect humans has been hampered by a lack of genetic information for three human-infective species:P. malariaeand twoP. ovalespecies (P. o. curtisiandP. o. wallikeri)1. These species are prevalent across most regions in which malaria is endemic2,3and are often undetectable by light microscopy4, rendering their study in human populations difficult5. The exact evolutionary relationship of these species to the other human-infective species has been contested6,7. Using a new reference genome forP. malariaeand a manually curated draftP. o. curtisigenome, we are now able to accurately place these species within thePlasmodiumphylogeny. Sequencing of aP. malariaerelative that infects chimpanzees reveals similar signatures of selection in theP. malariaelineage to anotherPlasmodiumlineage shown to be capable of colonization of both human and chimpanzee hosts. Molecular dating suggests that these host adaptations occurred over similar evolutionary timescales. In addition to the core genome that is conserved between species, differences in gene content can be linked to their specific biology. The genome suggests thatP. malariaeexpresses a family of heterodimeric proteins on its surface that have structural similarities to a protein crucial for invasion of red blood cells. The data presented here provide insight into the evolution of thePlasmodiumgenus as a whole.