Specific host–parasite interactions, where the outcome of exposure to a parasite depends upon the genotypic identity of both parties, have implications for understanding host–parasite coevolution and patterns of genetic diversity. Thus, grasping the extent to which these interactions are mediated by environmental changes in a spatially and temporally heterogeneous world is vital. In this study, it is shown that the environment can influence specific host–parasite interactions in the well-studied system of the bumblebee Bombus terrestris and its trypanosome parasite Crithidia bombi. Naturally relevant variation in the quality of the food environment formed a three-way interaction with both host and parasite identity in determining the outcome of infection, with regard to the resistance of the host and the transmission of the parasite. The demonstration of such a host-genotype by parasite-genotype by environment interaction (GH x GP x E) shows the importance of considering environmental variation when investigating host–parasite interactions. Moreover, such interactions may to some extent explain levels of genetic diversity in natural host–parasite systems owing to the fact that they will create selection mosaics when environments are heterogeneous.