Hosts of brood parasitic birds face reduced reproductive success as a direct consequence of rearing parasitic young. The most commonly evolved host behavior to combat costly parasitism is the rejection of foreign eggs. Despite consistent patterns of reduced nesting success in broods parasitized by brown-headed cowbirds (Molothrus ater), most of its host species do not reject foreign eggs. Paradoxically, where it is present, egg rejection is more common among cowbird hosts with larger body sizes, yet cowbird chicks are less likely to outcompete larger host nest mates. This raises a fundamental question whether egg rejection, even in the minority of cowbird hosts, has specifically evolved in response to costly brood parasitism. Here we tested predictions associated with this hypothesis in an egg-rejecter host, the American robin (Turdus migratorius), by assessing whether experimental cowbird parasitism causes reduced nesting success. We cross-fostered cowbird and control, host chicks into robin nests, testing for experimental effects of chick species, brood size, and hatching asynchrony; unmanipulated nests served as additional controls. Rearing a foreign chick in the brood reduced the reproductive output of host robins, however, we detected no effect of parasitizing host nests with a cowbird versus robin chick. Cowbird chicks were significantly less likely to fledge than cross-fostered robin chick controls. These experiments reveal that parasitism itself can exert a cost on robin hosts during the nestling stage, representing a recoverable cost of cowbird parasitism that can be avoided by the host through rejecting parasite eggs prior to hatching. These results support the assumption that foreign egg rejection is an evolved host response to brood parasitism in this system, despite the poor survival rate of cowbird chicks in robin broods.