In recent years, Japanese oak wilt causing mass mortality of oak trees has exhibited a significant geographical expansion. Understanding the formation history of current local populations of Platypus quercivorus Murayama, a vector of Japanese oak wilt, is important foundational knowledge for effectively preventing forest damage. In this study, we used genome-wide single nucleotide polymorphism data to infer the population genetic structure and historical demography of P. quercivorus populations in eastern Japan, where Japanese oak wilt is rapidly expanding.We found at least 3 distinct genetic groups, each of which caused Japanese oak wilt in different areas.The supported scenario suggests that 1 of 2 genetic groups in the northeast first diverged from the ancestral population, then the other group diverged from the southwestern population, followed by gene flow between the 2 groups. Recent admixtures of the 2 northeastern groups were identified at certain sites.The geographic genetic structure of the populations suggested that each genetic group experienced recent range expansion. Although genetically independent populations had caused oak tree mass mortality in their original distribution range, our results support the hypothesis that the recent geographic expansion of Japanese oak wilt outbreaks is attributed to the range expansion of these P. quercivorus groups.