Hybridization and genetic introgression can be associated with secondary contact between closely related species. Previous models have examined the ecological and demographic conditions leading to hybridization and introgression, but few have examined the role of behavior. Alternative mating behaviors are common throughout the animal kingdom but have rarely been recognized as a potential mechanism for hybridization. We developed an individual-based genetic model to examine the hypothesis that extra-pair copulations (EPCs) can lead to hybridization and genetic introgression even when assortative mating preferences are intact. Our model showed that female choice, whether pre- or post-copulation, reinforced species boundaries and that hybrids were relatively uncommon when no EPCs occurred. However, when EPCs were introduced into the model, the proportion of hybrids in the population depended on the strength of female mate or sperm choice, the strength of male pursuit of EPCs, and habitat-induced effects on the species composition of the neighborhood. As predicted, male pursuit of EPCs caused extensive introgression, but female preference for conspecific paternity reinforced species differences. Inclusion of mitochondrial markers of species identity revealed significant effects of interspecific and intersexual behavior during EPCs on the direction of introgression. These results suggest that an alternative mating tactic may have major effects on the level of genetic homogenization and can cause local extinction of a species.