Understanding the population dynamics and co-evolution of host–parasite systems requires detailed knowledge of their phenology which, in turn, requires a deep knowledge of the effect of abiotic factors on the life cycles of organisms. Temperature is known to be a key environmental influence that participates in the regulation of diapause. Yet, not much is known about the effect of temperature on the free-living stages of true parasites and how it may influence host–parasite interactions. Here we experimentally study the effect of ambient temperature on overwintering pupae of Carnus hemapterus (Diptera, Carnidae), an ectoparasitic fly of various bird species. We also test whether chilling is a prerequisite for completion of diapause in this species. In the course of three winter seasons we experimentally exposed carnid pupae from nests of various host species to spring temperatures with and without chilling and recorded the emergence patterns in experimental and control groups. Experimental groups showed an advanced emergence date, a lower emergence rate and, consequently, a protracted emergence period. Chilling had no obvious effect on the start of emergence but it did advance the mean emergence date, shortened the length of the emergence period when compared with the control treatment and increased the emergence rate when compared with the spring treatment. This study identifies an environmental cue, namely temperature during the free-living stage, affecting the emergence of a widespread parasite and demonstrates the plasticity of diapause in this parasite. Our findings are of potential significance in understanding host–parasite interactions.