Multiple parasitism of host nests by generalist brood parasites reflects the decisions of laying females and may influence the development and behavior of parasitic young. We used microsatellite and mtDNA control-region haplotype data to examine the relatedness of Brown-headed Cowbird (Molothrus ater) offspring in multiply parasitized nests sampled from a heavily parasitized host community in northeastern Kansas. We also examined how host nest availability influenced the degree of multiple parasitism, and used community-wide parasitism data to explore whether female cowbirds were constrained in their laying decisions. Relatedness estimates for all suitable pairwise comparisons (n = 94 from 41 multiply parasitized nests) found that the mean likelihood than an individual cowbird in a multiply parasitized nest shared its nest with a full sibling was 40.4% (95% confidence interval: 28.4–52.4%), indicating that many cowbird offspring were reared with full siblings. Extensive community-wide parasitism data revealed that most cowbird offspring shared the nest with ≥1 other conspecific. Additionally, we found that the proportion of available host nests increased steeply at the start of the breeding season and remained high for most of the breeding season, but that the degree of multiple parasitism was unrelated to the number of new nests. We found evidence that laying decisions of female cowbirds were constrained, which suggests that heavy parasitism levels were due to a high degree of competition for host nests. This intense competition for host nests, in turn, results in cowbird offspring often competing with conspecifics in our population, including full siblings, for host parental care.