Parasite dynamics can be mediated by host behaviours such as sociality, and seasonal changes in aggregation may influence risk of parasite exposure. We used little brown bats (Myotis lucifugus) captured during the autumn mating/swarming period to test the hypothesis that seasonal and demographic-based variation in sociality affect ectoparasitism. We predicted that ectoparasitism would: (1) be higher for adult females and young of the year (YOY) than adult males because of female coloniality; (2) increase for adult males throughout swarming because of increasing contact with females; (3) decrease for adult females and YOY throughout swarming because of reduced coloniality and transmission of individual ectoparasites to males; (4) be similar for male and female YOY because vertical transmission from adult females should be similar. Ectoparasitism was lowest for adult males and increased for males during swarming, but some effects of demographic were unexpected. Contrary to our prediction, ectoparasitism increased for adult females throughout swarming and YOY males also hosted fewer ectoparasites compared with adult and YOY females. Interestingly, females in the best body condition had the highest parasite loads. Our results suggest that host energetic constraints associated with future reproduction affect pre-hibernation parasite dynamics in bats.