Plasmodium vivax is responsible of the majority of malaria infections outside Africa. Its closer genetic relative, Plasmodium vivax-like, was discovered in African great apes and suggested to have given rise to P. vivax in humans. We generated two newly P. vivax-like reference genomes and 9 additional P. vivax-like genotypes, to unravel the evolutionary history of P. vivax. We showed a clear separation between the two clades, a higher genetic diversity of P. vivax-like parasites in comparison to the P. vivax ones, and the potential existence of two sub-clades of P. vivax-like. We dated the relative split between P. vivax and P. vivax-like as three times shorter than the split between P. ovale wallikeri and P. ovale curtesi and 1.5 times longer than the split between Plasmodium malariae. The sequencing of the P. vivax-like genomes is an undeniable advance in the understanding of P. vivax biology, evolution and emergence in human populations.