The molecular mechanisms by which parasites mediate host behavioral changes remain largely unexplored. Here, we examine Drosophila melanogaster infected with Wolbachia, a symbiont transmitted through the maternal germline, and find Wolbachia infection increases female receptivity to male courtship and hybrid mating. Wolbachia colonize regions of the brain that control sense perception and behavior. Quantitative global proteomics identify 177 differentially abundant proteins in infected female larval brains. Genetic alteration of the levels of three of these proteins in adults, the metabotropic glutamate receptor mGluR, the transcription factor TfAP-2, and the odorant binding protein Obp99b, each mimic the effect of Wolbachia on female receptivity. Furthermore, >700 Wolbachia proteins are detected in infected brains. Through abundance and molecular modeling analyses, we distinguish several Wolbachia-produced proteins as potential effectors. These results identify potential networks of host and Wolbachia proteins that modify behavior to promote mating success and aid the spread of Wolbachia.