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Barley (<i>Hordeum vulgare</i> L.) is the most important cereal crop in the Qinghai-Tibet Plateau, and the yield has been seriously threatened by <i>Blumeria graminis</i> f. sp. <i>hordei</i> (<i>Bgh</i>) in recent years. To understand the virulence and genetic traits of different <i>Bgh</i> populations, 229 isolates of <i>Bgh</i> were collected from Tibet, Sichuan, Gansu and Yunnan provinces of China during 2020 and 2021, and their pathogenicity to 21 barley lines of different genotypes was assessed. A total of 132 virulent types were identified. The <i>Bgh</i> isolates from Yunnan showed the highest diversity in terms of virulence complexity (<i>Rci</i>) and genetic diversity (<i>KWm</i>), followed by those from Sichuan, Gansu, and Tibet, in that order. Single nucleotide polymorphism (SNP) in genes coding for alternative oxidase (AOX), protein kinase A (PKA), and protein phosphatase type 2A (PPA) were detected at seven polymorphic sites. Nine haplotypes (H1–H9) with an average haplotype diversity (<i>Hd</i>) and nucleotide diversity π of 0.564 and 0.00034, respectively, were observed. Of these, haplotypes H1 and H4 accounted for 88.8% of the isolates, and H4 was predominant in Tibet. Genetic diversity analysis using the STRUCTURE (K = 2) and AMOVE indicated that the inter-group variation accounted for 54.68%, and inter- and intra-population genotypic heterogeneity accounted for 23.90% and 21.42%, respectively. The results revealed the recent expansion of the <i>Bgh</i> population in Tibet, accompanied by an increase in virulence and a loss of genetic diversity.