Plasmodium vivaxcauses >70% of malaria cases in Latin America. The emergence ofPlasmodium simium, transmitted from humans to monkeys, increased the malaria burden, notably after an outbreak in 2015 in Brazil. To investigateP. simiumevolutionary history, we screened 646 monkey samples and analyzed whole genome variations for 19P. simiumand 408P. vivaxisolates.P. vivaxstrains were identified in Colombian (n=3) and Brazilian monkeys (n=1), suggesting host reinvasion in Colombia and genetic exchange betweenP. vivaxandP. simiumin Brazil. Genetic analysis indicates thatP. simiumoriginated from a host jump approximately a century ago, possibly linked toP. vivaxmigration from Mexico to Brazil. Genome-wide scans identified selection in genes interacting with primate hosts and vectors. These findings highlightP. simiumevolutionary history and zoonotic malaria risks, and underscore the need to include monkeys in malaria prevention measures while ensuring human-wildlife coexistence.