Organisms and their natural enemies can have dynamic coevolutionary trajectories, but anthropogenic effects like species introductions interrupt existing coevolutionary relationships. For parasites in particular, if they are introduced to a location without their hosts, they can only persist in the new environment if alternative hosts are 1) present, 2) detectable to parasites, and 3) capable of sustaining parasites. The circumstances surrounding the addition of alternative hosts to a parasite’s repertoire are rarely observed. The parasitoid fly Ormia ochracea locates its field cricket hosts by orienting acoustically to their conspicuous mating songs. In Hawaii, O. ochracea is only known to parasitize one species, Teleogryllus oceanicus, but rapid evolution of T. oceanicus mating song over the past 20 years has led to several prevalent morphs of the cricket that produce no song or novel songs that the flies cannot detect. Yet flies persist in populations that lack ancestral singing T. oceanicus, prompting us to investigate the possibility of alternative hosts in Hawaii. We demonstrate first that three potential alternative hosts (Gryllodes sigillatus, Gryllus bimaculatus, and Modicogryllus pacificus) are present. Second, O. ochracea exhibits a positive phonotactic response to all three species’ songs in the field and in the lab. And third, O. ochracea can successfully develop to pupae and emerge as adults in all three species. Our discovery of alternative hosts for O. ochracea in Hawaii infuses the system with intriguing complexity and offers extensive opportunities for future work.