Native insects can become epidemic pests in agro-ecosystems. A population genetics approach was applied to analyze the emergence and spread of outbreak populations of native insect species. Outbreaks of the mirid bug, Stenotus rubrovittatus, have rapidly expanded over Japan within the last two decades. To characterize the outbreak dynamics of this species, the genetic structure of local populations was assessed using polymorphisms of the mtDNA COI gene and six microsatellite loci. Results of the population genetic analysis suggested that S. rubrovittatus populations throughout Japan were genetically isolated by geographic distance and separated into three genetic clusters occupying spatially segregated regions. Phylogeographic analysis indicated that the genetic structure of S. rubrovittatus reflected post-glacial colonization. Early outbreaks of S. rubrovittatus in the 1980s occurred independently of genetically isolated populations. The genetic structure of the populations did not fit the pattern of an outbreak expansion, and therefore the data did not support the hypothesis that extensive outbreaks were caused by the dispersal of specific pestiferous populations. Rather, the historical genetic structure prior to the outbreaks was maintained throughout the increase in abundance of the mirid bug. Our study indicated that changes in the agro-environment induced multiple outbreaks of native pest populations. This implies that, given suitable environmental conditions, local populations may have the potential to outbreak even without invasion of populations from other environmentally degraded areas.