Immunologists and evolutionary biologists are interested in how the immune system evolves to fit an ecological niche. We studied the relationship between exposure to parasites and strength of immunity by investigating the response of two species of New World cowbirds (genus Molothrus, Icteridae), obligate brood parasites with contrasting life history strategies, to experimental arboviral infection. The South American shiny cowbird (M. bonariensis) is an extreme host-generalist that lays its eggs in the nests of >225 different avian species. The Central American bronzed cowbird (M. aeneus) is a relative host-specialist that lays its eggs preferentially in the nests of approximately 12 orioles in a single sister genus. West Nile virus provided a strong challenge and delineated immune differences between these species. The extreme host-generalist shiny cowbird, like the North American host-generalist, the brown-headed cowbird, showed significantly lower viremia to three arboviruses than related icterid species that were not brood parasites. The bronzed cowbird showed intermediate viremia. These findings support the interpretation that repeated exposure to a high diversity of parasites favors the evolution of enhanced immunity in brood parasitic cowbirds and makes them useful models for future studies of innate immunity.