Apple scab, caused by Venturia inaequalis, is a destructive fungal disease of major apple cultivars worldwide, most of which are moderately to highly susceptible. Thus, development of scab resistant cultivars is one of the highest priorities of apple breeding programs. The principal source of resistance for breeding programs has been the scab resistance gene Rvi6 that originated from the Japanese crabapple Malus floribunda (Sieb.) sel. 821. Isolates of V. inaequalis able to overcome Rvi6 have been identified in Europe, but have not yet been reported on the American continents. We recently discovered scab infection on M. floribunda 821 trees in a research orchard at Geneva, NY, U.S.A., where approximately 10% of the leaves bore profusely sporulating apple scab lesions, many of which had coalesced to cover entire leaves. We observed both chlorosis, typical to Rvi6, and pinpoint pitting symptoms typical to failed infections by V. inaequalis on hosts bearing the Rvi7 gene. We assessed genetic diversity and population genetic structure of 11 V. inaequalis isolates in total, of North American and European origin, isolated from M. floribunda 821, ‘Nova Easygro’, ‘Golden Delicious’, TSR33T239, ‘Schone van Boskoop’, and ‘Prima’, using 16,321 genome-wide SNPs. Population genetic structure and PCA separated the isolates into distinct European and U.S. groups. The forgoing suggests that the new Rvi6 virulent isolates emerged within U.S. populations, rather than being transported from Europe. The complete resistance breakdown in M. floribunda 821 but not in descendant cultivars, which kept their field resistance, suggests that durable resistance to apple scab will require a more comprehensive understanding of Rvi6 mediated resistance in diverse genetic backgrounds.