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Abstract Relatively little is known about the processes shaping population structure in cooperatively breeding insect species, despite the long-hypothesized importance of population structure in shaping patterns of cooperative breeding. Polistes paper wasps are primitively eusocial insects, with a cooperative breeding system in which females often found nests in cooperative associations. Prior mark-recapture studies of Polistes have documented extreme female philopatry, although genetic studies frequently fail to detect the strong population structure expected for highly philopatric species. Together these findings have led to lack of consensus on the degree of dispersal and population structure in these species. This study assessed population structure of female Polistes fuscatus wasps at three scales: within a single site, throughout Central New York, and across the Northeastern United States. Patterns of spatial genetic clustering and isolation by distance were observed in nuclear and mitochondrial genomes at the continental scale. Remarkably, population structure was evident even at fine spatial scales within a single collection site. However, P. fuscatus had low levels of genetic differentiation across long distances. These results suggest that P. fuscatus wasps may employ multiple dispersal strategies, including extreme natal philopatry as well as longer-distance dispersal. We observed greater genetic differentiation in mitochondrial genes than in the nuclear genome, indicative of increased dispersal distances in males. Our findings support the hypothesis that limited female dispersal contributes toward population structure in paper wasps.