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Parasite infestation may impose direct costs of blood, nutrient, and energy depletion, along with indirect costs of increased immune response upon hosts. We investigated how ectoparasitism influences body mass and reproduction in a free-living population of Franklin’s ground squirrels (Poliocitellus franklinii (Sabine, 1822)) located near Delta Marsh, Manitoba, Canada. We experimentally reduced ectoparasite burden by treating seven reproductive females with an insecticide following breeding and contrasted body mass and reproductive performance of those individuals to seven sham-treated control females. Insecticide-treated dams did not differ from sham-treated dams in body mass, litter size, or juvenile mass, and thus, dam growth and reproduction were not compromised by ectoparasite defense at the infestation levels experienced in this study. However, litter sex ratio differed significantly between insecticide-treated and control females, with a higher proportion of male offspring produced among females with reduced ectoparasite load. Our findings are thus consistent with the Trivers–Willard model for adaptive sex allocation, yet they provide novel comparative insight into how sociality may modulate the expression of adaptive sex allocation among small mammals given the differential payoff associated with the production of high-quality female versus male offspring in more social versus less social species.