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Plague, one of the most devastating infectious diseases in human history, is caused by the bacterium Yersinia pestis. Since the 1950s, the Dehong Dai–Jingpo Autonomous Prefecture (DH) in Yunnan Province, China, has recorded plague outbreaks that have resulted in 1,153 human cases and 379 deaths. The genetic diversity and transmission characteristics of Y. pestis strains in this region remain unknown. Here, we performed high-resolution genomic epidemiological analysis of 175 Y. pestis strains isolated from five counties and 19 towns in DH between 1953 and 2007. Phylogenetic analysis revealed that most DH strains were located in lineage 1.ORI2, which could be further subdivided into seven sub-phylogroups (SPG1-SPG7). The dominant sub-phylogroups of Y. pestis in DH varied during different periods and presented a population shift. Genomic evidence showed that plague might have emerged from the southwest of DH (e.g., Longchuan or Ruili counties) or its bordering countries, and subsequently spread to the northeast in multiple waves between 1982 and 2007. Our study infers a fine-scale phylogeny and spread pattern of the DH Y. pestis population, which extends our knowledge regarding its genetic diversity and provides clues for the future prevention and control of plague in this region. Author summary: Yersinia pestis, the causative agent of plague, has led to three historic pandemics and remains a major public health issue. Here, genomic epidemiological analysis of 175 Y. pestis strains isolated over 50 years from the Dehong Dai—Jingpo Autonomous Prefecture, a region located in southwestern China, revealed the genomic evolution scenario of Y. pestis with high resolution. Our results revealed that plague epidemics in this region were led by different phylogroups, and population shift events were observed during different years, suggesting high dynamics of Y. pestis populations in the local natural plague foci. We found that the spread of plague was from southwest to northeast and inferred the possible origin of the epidemics, which would help strengthen surveillance of the epizootic in local natural plague foci and promote the prevention and control of human plague. [ABSTRACT FROM AUTHOR]