Apple scab caused by Venturia inaequalis is the most threatening plant disease in Aomori Prefecture, which receives heavy snowfall. Here, we collected 169 monoconidial isolates of V. inaequalis from Tsugaru (6 orchards) and Nanbu regions (3 orchards) in Aomori Prefecture, Japan, and analyzed their genetic diversity and population structure using 15 microsatellite markers. One hundred and six alleles were detected, ranging from 3 to 17 alleles per locus. Genetic diversity analysis showed high variability from 0.35 to 0.85. One hundred and sixty-six haplotypes were detected, suggesting that genetic recombination occurred at a high frequency. In a principal coordinate analysis, V. inaequalis isolates from the Tsugaru and Nanbu regions showed partial overlap and no distinct clusters. In a structure analysis, the optimal population number (K) was estimated to be 2. One of the estimated populations consisted of 83% Nanbu isolates and the other of 71% Tsugaru isolates, supporting the occurrence of geographically defined populations. Pairwise genetic differentiation between orchards showed a wide range within the Tsugaru population, whereas the lowest values were observed between the Tsugaru and Nanbu orchards. This result suggests a link between geographic distance and gene flow, suggesting long-distance movement between populations via nursery plants. This report using microsatellite markers is the first analysis of the population genetics of V. inaequalis in Aomori.