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Background: Fleas are the most economically significant blood-feeding ectoparasites worldwide. Ctenocephalides felis and Pulex irritans can parasitize various animals closely related to humans and are of high veterinary significance. Methods: In this study, 82 samples were collected from 7 provinces of China. Through studying the nuclear genes ITS1 and EF-1α and two different mitochondrial genes cox1 and cox2, the population genetics and genetic variation of C. felis and P. irritans in China were further investigated. Results: The intraspecies differences between C. felis and P. irritans ranged from 0 to 3.9%. The interspecific variance in the EF-1α, cox1, and cox2 sequences was 8.2–18.3%, while the ITS1 sequence was 50.1–52.2%. High genetic diversity was observed in both C. felis and P. irritans, and the nucleotide diversity of cox1 was higher than that of cox2. Moderate gene flow was detected in the C. felis and P. irritans populations. Both species possessed many haplotypes, but the haplotype distribution was uneven. Fu's Fs and Tajima's D tests showed that C. felis and P. irritans experienced a bottleneck effect in Guangxi Zhuang Autonomous Region and Henan province. Evolutionary analysis suggested that C. felis may have two geographical lineages in China, while no multiple lineages of P.irritans were found. Conclusions: Using sequence comparison and the construction of phylogenetic trees, we found a moderate amount of gene flow in the C. felis and P. irritans populations. Both species possessed many haplotypes, but the distribution of haplotypes varied among the provinces. Fu's Fs and Tajima's D tests indicated that both species had experienced a bottleneck effect in Guangxi and Henan provinces. Evolutionary analysis suggested that C. felis may have two geographical lineages in China, while no multiple lineages of P.irritans were found. This study will help better understand fleas' population genetics and evolutionary biology. [ABSTRACT FROM AUTHOR]