Host-parasite interactions are a key paradigm for understanding the process of coevolution. Central to coevolution is how genetic variation in interacting species allows parasites to evolve manipulative strategies. However, genetic variation in the parasite may also be associated with host phenotype changes, thereby changing the selection on both species. For instance, parasites often induce changes in the behaviour of their host to maximize their own fitness, yet the quantitative genetic basis for behavioural manipulation has not been fully demonstrated. Here, we show that the genotype of the parasitoid wasp Aphidius ervi has a significant effect on where its aphid host Acyrthosiphon pisum moves to die following parasitism, including the likelihood that the aphid abandons the plant. These results provide a clear example of an interspecific indirect genetic effect whereby the genetics of one species influences the expression of a specific behavioural trait in another.