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Wheat leaf rust, caused by <i>Puccinia triticina</i>, is one of the most common fungal diseases of wheat in China and occurs widely in various wheat-growing regions. To clarify the epidemic, spread rules, and population structure of <i>P. triticina</i> among different regions, 217 isolates of <i>P. triticina</i> collected from Hebei, Shandong, Sichuan, and Xinjiang in China were tested by 34 Thatcher near-isogenic lines and 21 pairs of EST-SSR primers. A total of 83 races were identified, and THTT, PHTT, THTS, and PHJT were the most predominant races in the four provinces in 2009. We found enriched virulence and genetic diversity in the four <i>P. triticina</i> populations and a significant correlation between genetic polymorphism and geographic regions. However, no significant correlation was found between virulence phenotypes and molecular genotypes. Moreover, a notable high level of gene flow (<i>N_m</i> = 2.82 > 1) among four <i>P. triticina</i> populations was detected. The genetic relationship among Hebei, Shandong, and Sichuan populations was close, possibly due to the spread of <i>P. triticina</i> from Sichuan to Shandong and then to Hebei. In contrast, the Xinjiang population was relatively independent. Genetic differentiation analysis showed some level of differentiation among or within populations of <i>P. triticina</i> in the four provinces, and the genetic variation within populations (74.97%) was higher than across populations (25.03%). Our study provides a basis for a better understanding of the regional migration, epidemic, and population structure of <i>P. triticina</i> in China.