Individuals of many species show high levels of fidelity to natal populations, often due to reliance on patchily distributed habitat features. In many of these species, the negative impacts of inbreeding are mitigated through specialized behaviours such as seasonal mating dispersal. Quantifying population structure for species with these characteristics can potentially elucidate social and environmental factors that interact to affect mating behaviour and population connectivity. In the northern part of their range, timber rattlesnakes are communal hibernators with high natal philopatry. Individuals generally recruit to the same hibernaculum as their mother and remain faithful to that hibernaculum throughout their lives. We examined the genetic structure of Crotalus horridus hibernacula in the northeastern USA using microsatellite loci. Sampled hibernacula exhibited only modest levels of differentiation, indicating a significant level of gene flow among them. We found no significant correlation between genetic differentiation and geographical distance, but did find significant positive correlation between genetic differentiation and a cost-based distance metric adjusted to include the amount of potential basking habitat between hibernacula. Therefore, thermoregulation sites may increase gene flow by increasing the potential for contact among individuals from different populations. Parentage analyses confirmed high levels of philopatry of both sexes to their maternal hibernaculum; however, approximately one-third of paternity assignments involved individuals between hibernacula, confirming that gene flow among hibernacula occurs largely through seasonal male mating dispersal. Our results underscore the importance of integrating individual-level behaviours and landscape features with studies of fine-scale population genetics in species with high fidelity to patchily distributed habitats.