Monogamy is rare among mammals and molecular investigations have revealed that many socially monogamous species participate in extrapair mating. The North American beaver (Castor canadensis) is a socially monogamous species that exhibits classic monogamous behavior, generally living in discrete colonies composed of a mated pair and their offspring. We examined genetic relationships within and among beaver colonies for 2 populations in Illinois to investigate average relatedness within colonies, occurrences of extrapair mating within or between colonies, and the influence of geographic distance on intercolony relatedness. Seven microsatellite loci developed for the beaver were used to estimate relatedness and parentage for 55 beavers in central Illinois and 72 beavers in southern Illinois. Average within-colony relatedness varied widely in both populations, ranging from 0.04 to 0.64 in central Illinois and from 0.16 to 0.41 in southern Illinois. Colonies were composed primarily of 1st- and 2nd-order relatives, but included unrelated individuals. Paternity analysis revealed that 5 (56%) of 9 litters had been sired by ≥2 males. Extrapair mating frequently occurred between members of neighboring colonies in southern Illinois. In contrast to long-held views that beavers are genetically monogamous and colonies are typically 1st-order relatives, we documented a wide range of relationships among colony members and multiple paternity in >50% of litters.