Continued use and development of new insecticides are seen as a necessary part of modern agriculture, but insecticides, even at sublethal levels, may also affect beneficial non-target species, such as pollinators, predators, and parasitic wasps. Here, we studied sublethal effects of four insecticides – acetamiprid, dimethoate, flupyradifurone, and sulfoxaflor – all targeting cholinergic neurons in insects, on sexual communication and olfactory host finding in the parasitic wasp Lariophagus distinguendus (Förster) (Hymenoptera: Pteromalidae). We found that all four insecticides reduced, at least at one of the tested sublethal doses, pheromone-mediated courtship behaviour (wing fanning) in males and the mating frequency of treated wasps. Treated females no longer preferred host-associated kairomones. This suggests that the olfactory sense of the wasps is hampered by sublethal insecticide doses. The lowest bioactive doses tested in the bioassays were 0.021 ng for sulfoxaflor and 0.105 ng for acetamiprid, dimethoate, and flupyradifurone. These low amounts are field realistic and might be taken up by the wasps, e.g., by feeding contaminated plant nectar. Exposure to these compounds likely compromises the important ecosystem service provided by parasitic wasps as natural enemies in terrestrial ecosystems.