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The malaria parasite Plasmodium malariae infects humans across Africa, Asia and South America, and has relatives infecting monkeys in the New World (Plasmodium brasilianum) and apes in Africa (Plasmodium rodhaini). The genetic relationships among these parasites, and even whether they represent separate species, are unclear. Combining DNA sequences newly derived from ape faecal and blood samples with others obtained by mining Plasmodium sequence read databases, we have investigated the evolutionary history of P. malariae and its relatives. We find that this group of parasites comprises three distinct lineages, one of which represents a previously unknown, distantly related species that infects wild-living chimpanzees, bonobos and gorillas across central and west Africa; we were able to assemble a very partial genome sequence (~500 kb) for this parasite. A second lineage infecting apes is much more closely related to human P. malariae, but there was little evidence of genetic exchange between the ape and human parasites, suggesting that these should be considered separate species. Patterns of nucleotide polymorphism suggest that the human parasite has undergone a severe genetic bottleneck, followed by population expansion. Together, these data suggest that the P. malariae lineage has a long history in Africa, and the human parasite may have arisen through a recent cross-species transmission from apes. Finally, our analysis places P. brasilianum as a lineage within the radiation of human P. malariae strains, confirming that P. brasilianum emerged following a recent anthroponotic transmission to New World monkeys.