We characterized several equivocal aspects of the breeding biology of the brood parasitic Brown-headed Cowbird (Molothrus ater) at a study site in northeastern Illinois. A total of 175 offspring and a partial sample of parents were sampled and genotyped at six microsatellite loci. A combination of sibling-group and parentage assignment enabled us to characterize mating behavior and area used for reproduction by breeding adults, even for those not sampled. We assigned a mean of 4.7 (range 1–13) and 4.4 (range 1–16) offspring to 33 female and 32 male parents, respectively. Adults typically reproduced with a “primary partner” but up to three partners were common. Offspring females and males were spread over 9 and 12 ha, respectively. Half of the polygynous males produced offspring with an additional mate that parasitized nests near to or within areas overlapping those of their primary partner. That suggests that mate choice takes place at females' egg-laying areas as opposed to more remote social areas. Multiple females frequently parasitized a single host nest and areas used for reproduction overlapped extensively for individuals of either sex. High frequencies of parasitism and superparasitism indicate a high cowbird density relative to that of hosts. Frequent promiscuity by cowbirds at our site contrasts with other studies reporting monogamy and may be due to higher densities of breeding cowbirds at our site.