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Abstract Malaria-causing protozoa of the genusPlasmodiumhave exerted one of the strongest selective pressures on the human genome, and resistance alleles provide biomolecular footprints that outline the historical reach of these species¹. Nevertheless, debate persists over when and how malaria parasites emerged as human pathogens and spread around the globe^1,2. To address these questions, we generated high-coverage ancient mitochondrial and nuclear genome-wide data fromP. falciparum,P. vivaxandP. malariaefrom 16 countries spanning around 5,500 years of human history. We identifiedP. vivaxandP. falciparumacross geographically disparate regions of Eurasia from as early as the fourth and first millenniabce, respectively; forP. vivax, this evidence pre-dates textual references by several millennia³. Genomic analysis supports distinct disease histories forP. falciparumandP. vivaxin the Americas: similarities between now-eliminated European and peri-contact South American strains indicate that European colonizers were the source of AmericanP. vivax, whereas the trans-Atlantic slave trade probably introducedP. falciparuminto the Americas. Our data underscore the role of cross-cultural contacts in the dissemination of malaria, laying the biomolecular foundation for future palaeo-epidemiological research into the impact ofPlasmodiumparasites on human history. Finally, our unexpected discovery ofP. falciparumin the high-altitude Himalayas provides a rare case study in which individual mobility can be inferred from infection status, adding to our knowledge of cross-cultural connectivity in the region nearly three millennia ago.