Technical Abstract: The structure of the U.S. wheat powdery mildew population (Blumeria graminis f. sp. tritici) has not been investigated, and the global evolutionary history of B. g. tritici is largely unknown. After gathering 141 single-ascoporic B. g. tritici isolates from 10 eastern U.S. locations, 34 isolates from the United Kingdom, and 28 isolates from Israel, we analyzed pathogen population structure using presumptively neutral markers. DNA was extracted, and primers for 12 “housekeeping” genes were designed and examined for polymorphism. Four of those genes were found to contain a total of 12 single-nucleotide polymorphisms (SNPs) in the U.S. population, and were also analyzed in the U.K. and Israeli populations. In total, 25 haplotypes were inferred from the four concatenated genes, with two of the haplotypes comprising over 70% of the U.S. population. Using Hudson’s tests and analysis of molecular variance (AMOVA), we found the wheat mildew isolates subdivided into four distinct regions: the Mid-Atlantic U.S., the southern U.S., the U.K., and Israel. Genotypic diversity was greatest in the U.K., Israel, Virginia, and Kinston, North Carolina, population samples. Using rarefaction, a procedure that compensates for differing sample sizes, we found that the cooler locations with greater conduciveness to regular powdery mildew epidemics had the greatest haplotype richness. Our results suggest that the eastern U.S. B. g. tritici population is young, descended recently from Old World populations with isolation and genetic drift, and is currently subdivided from north to south.