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Background: The ambrosia beetle, Platypus quercivorus, is the vector of oak wilt, one of the most serious forest diseases in Japan. Population genetics approaches have made great progress toward studying the population dynamics of pests, especially for estimating dispersal. Knowledge of the genetic structuring of the beetle populations should reveal their population history. Using five highly polymorphic microsatellite loci, 605 individuals from 14 sampling sites were assessed to infer the ongoing gene flow among populations as well as the processes of expansion of damaged areas., Results: Population differentiation (FST = 0.047, G'ST = 0.167) was moderate and two major clusters were detected by several methods, dividing the samples into north-eastern and south-western populations, a similar genetic divergence was reported in host oak trees. Within the north-eastern populations, the subgroups mostly corresponded to differences in the collection period. The genetic characteristics of the population might have changed after 2 years due to the mixing of individuals between populations with enhanced migration related to population outbreaks. Because isolation by distance was detected for whole populations and also within the north-eastern populations, migration was considered to be limited between neighbouring populations, and most populations were suggested to be in genetic equilibrium of genetic drift and gene flow. Recent bottlenecks were found in some populations with no geographical bias; however, they were all from newly emerged oak wilt forests. The emergence of oak wilt should have induced intense fluctuations in the beetle population size., Conclusions: Because the genetic boundaries coincide, we suggest that the geographical structuring of the beetle was formed by co-evolution with the host species. Our findings indicate the oak wilt expansion process.