Many parasites require synchronization of their infective phases with the appearance of susceptible host individuals and, for many species, diapause is one of the mechanisms contributing to such coincidence. A variety of ecological factors, like changes in host temperature produced by involuntary host shifting (substitution of the usual host by an infrequent one), can modify host-parasite synchronization of diapausing ectoparasites of endothermic species. To understand the influence of host shifting on the mechanisms of parasite synchronization, we conducted experiments using the system formed by the ectoparasitic fly Carnus hemapterus and its avian hosts. We simulated the occurrence of the usual host and natural cases of host shifting by exposing overwintering carnid pupae from Bee-eater nests (Merops apiaster) to the earlier incubation periods of two Carnus host species that frequently reoccupy Bee-eater nests. Pupae exposed to host shifting treatments advanced the mean date of emergence and produced an earlier and faster rate of emergence in comparison with pupae exposed both to the control (absence of any host) and Bee-eater treatments. The effect was more evident for the treatment resembling the host with the most dissimilar phenology to the one of the usual host. Our results show that host temperature is an environmental cue used by this nest-dwelling haematophagous ectoparasite and reveal that Carnus hemapterus has some potential to react to involuntary host shifting by means of plasticity in the termination of diapause.