Wild birds play a key role in the amplification and transmission of many of the arthropod-borne viruses (arboviruses). Determining the extent to which birds are affected by these viruses is critical in predicting the pathogens' spread or maintenance in vertebrate host populations. Little is known about how arboviruses affect amplifying hosts' fitness, especially in cases where these viruses infect nestling birds. Buggy Creek virus (BCRV; Togaviridae: Alphavirus) is an RNA arbovirus transmitted by the Swallow Bug (Oeciacus vicarius) to Cliff Swallows (Petrochelidon pyrrhonota) and House Sparrows (Passer domesticus) that have recently occupied Cliff Swallow nesting colonies. We examined fitness, as measured by fledging success, of House Sparrows occupying Cliff Swallow nesting colonies in western Nebraska. Most nestlings naturally infected by BCRV at 4–6 days of age died, and even older nestlings, when infected, showed fledging success of <40%. Whether ≥1 nestling in a brood was infected with BCRV was the most important determinant of nest success in this population. Colony sites with high BCRV prevalence had lower rates of nest success, and surviving broods at those sites were smaller. Although most infected nestling House Sparrows eventually die, they survive long enough to infect Swallow Bugs, and in this way they play a critical role in BCRV transmission. Frequent emigration of unexposed House Sparrows into these colonies and their renesting throughout the summer leads to these sites being perpetual foci for BCRV epizootics. Few other arboviruses are known to have such extreme effects on the fitness of their vertebrate hosts.