Within parasite communities infecting the same host, ecological theory predicts that two species occupying the same niche should evolve distinct niche use to avoid direct competition. Biological invasions can however create situations, where competition could not select for different niche occupancy and closely related parasites species find themselves competing for the same host resources for the first time since their lineages split. Such novel interactions cannot only alter the evolutionary trajectories of both parasite species, but will also feed back on the immune response of the host. Here, we show how the invasion of the parasitic copepod Mytilicola orientalis creates competition with the established congeneric parasite Mytilicola intestinalis, and how this novel menage a trois feeds back on the immune response of the blue mussel host Mytilus edulis. From a series of controlled infection experiments that manipulate competition among the parasites we can show that, although both species occur in the same section of the mussel gut, competition between the parasites is weak and shows similar impact on host condition in either simultaneous or sequential infections. Triplet transcriptomics of matching host (M. edulis) and parasite samples (M. intestinalis and M. orientalis) however revealed that the novel interaction of the invader with the host changes the transcriptional activity of many more genes and processes than the interaction with the established and coevolved parasite. Our results therefore not only show the utility of biological invasions of parasites to study coevolutionary processes, but also shows that responses to novel host-parasite interactions can lead to massive reactions on the molecular level that are not reflected in host or parasite phenotypes.