A largely unanswered question in the study of arboviruses is the extent to which virus can overwinter in adult vectors during the cold winter months and resume the transmission cycle in summer. Buggy Creek virus (BCRV; Togaviridae, Alphavirus) is an unusual arbovirus that is vectored primarily by the swallow bug (Hemiptera: Cimicidae: Oeciacus vicarius) and amplified by the ectoparasitic bug's main avian hosts, the migratory cliff swallow (Petrochelidon pyrrhonota) and resident house sparrow (Passer domesticus). Bugs are sedentary and overwinter in the swallows' mud nests. We evaluated the prevalence of BCRV and extent of infection in swallow bugs collected at different times in winter (October-early April) in Nebraska and explored other ecological aspects of this virus's overwintering. BCRV was detected in 17% of bug pools sampled in winter. Virus prevalence in bugs in winter at a site was significantly correlated with virus prevalence at that site the previous summer, but winter prevalence did not predict BCRV prevalence there the following summer. Prevalence was higher in bugs taken from house sparrow nests in winter and (in April) at colony sites where sparrows had been present all winter. Virus detected by reverse transcription (RT)-polymerase chain reaction in winter was less cytopathic than in summer, but viral RNA concentrations of samples in winter were not significantly different from those in summer. Both of the BCRV lineages (A, B) overwintered successfully, with lineage A more common at sites with house sparrows and (in contrast to summer) generally more prevalent in winter than lineage B. BCRV's ability to overwinter in its adult vector probably reflects its adaptation to the sedentary, long-lived bug and the ecology of the cliff swallow and swallow bug host-parasite system. Its overwintering mechanisms may provide insight into those of other alphaviruses of public health significance for which such mechanisms are poorly known.