In many social sciurids, male territoriality confers significant mating advantages. We evaluated resident male paternity in Gunnison's prairie dogs (Cynomys gunnisoni), a colonial ground-dwelling sciurid, where males and females cooperatively defend territories. Contrary to findings reported for other social sciurids, our results show that territorial resident males do not gain significant reproductive advantages. Resident males sired the majority of offspring from their respective territories only 10.5% of the time. A single non-resident male sired equal or greater number of offspring than any single resident male 71.2% of the time. While adult males were more likely to sire a greater number of offspring, standard heterozygosity, body mass, and territory size were not significant predictors of how many offspring a male sired. In addition, the number of other males present did not influence the number of offspring sired by any given resident male. However, territory size was significantly correlated with overall offspring number and mean litter size per female, suggesting a potential reproductive advantage for females that occupy larger, better quality territories. Previous work has demonstrated that the cooperative defence of territories by both males and females permits enhanced access to food resources critical to overwinter survival. Our results have important implications for studies that do not distinguish between social and mating systems, because they suggest that individual mating strategies may be different from the social strategies that emerge in response to resource availability.