Potato virus Y (PVY) has emerged as a significant problem in all potato-producing areas, including North America. PVY exists as a complex of strains producing a range of disease symptoms in various potato cultivars leading to yield reduction, and some of these strains are known to affect tuber quality. In the past 30 years, significant changes in PVY strains circulating in potato crops have been observed in Europe, and more recently in North America, with an increased incidence of PVY strains associated with potato tuber damage. Different models have been proposed to explain these changes, including spread of new recombinants, enhanced vector transmission of certain strains, or introduction of new potato varieties. Here, we analyze the current knowledge of PVY genetic diversity with an emphasis on PVY strains common in North America. Multiple types of PVY genome recombinants with links to specific symptoms in potato varieties are described and discussed. Different approaches to distinguish PVY strains are reviewed and compared, including biological and laboratory methods.