Abstract Potato virus Y (PVY) exists as a complex of strains, including a growing number of recombinants. Evolution of PVY proceeds through accumulation of mutations and more rapidly through recombination. Here, the role of recombination in PVY evolution and the origin of common PVY recombinants were studied through whole genome analysis of 119 newly sequenced PVY isolates largely from U.S. potato, and subsequent combined phylogenetic and recombination analyses with an additional 166 whole PVY genomes from the GenBank database. Two novel PVYC recombinants were sequenced and identified, along with one novel PVYN:O recombinant. Sequence diversity in the parental sequences made it possible to trace the origins of all recombinant types of PVY, which also showed remarkable sequence diversity in most cases. The results suggested that the common recombinant PVY strains originated more than once, from different parental sequences.