In modern agriculture, control of insect pests is achieved by using insecticides that can also have lethal and sublethal effects on beneficial non-target organisms. Here, we investigate acute toxicity and sublethal effects of four insecticides on the males’ sex pheromone response and the female host finding ability of the Drosophila parasitoid Leptopilina heterotoma. The nicotinic acetylcholine receptor antagonists acetamiprid, flupyradifurone and sulfoxaflor, as well as the acetylcholinesterase inhibitor dimethoate were applied topically as acetone solutions. Males treated with all four insecticides no longer preferred the female sex pheromone in a T-olfactometer. Duration of wing fanning, an element of the pheromone-mediated male courtship behavior, was also reduced by all four insecticides. The ability of females to orientate towards host-infested feeding substrate was not affected by acetamiprid in the tested dose range. However, treatment with dimethoate, flupyradifurone and sulfoxaflor resulted in the loss of the females’ preference for host odor. At the lowest doses interfering with olfactory abilities of L. heterotoma in this study (acetamiprid: 0.21 ng, dimethoate: 0.105 ng, flupyradifurone: 2.1 ng and sulfoxaflor: 0.21 ng), ≥ 90% of the wasps survive insecticide treatment. Male pheromone responses and female host finding were also disturbed in those L. heterotoma that had developed in D. melanogaster larvae reared on dimethoate-treated feeding medium at sublethal levels. Hence, doses of this insecticide sufficient to interfere with chemical orientation of L. heterotoma can be taken up by the parasitoid via the food chain.