Individual variation in social behavior seems ubiquitous, but we know little about how it relates to brain diversity. Among monogamous prairie voles, levels of vasopressin receptor (encoded by the geneavprla) in brain regions related to spatial memory predict male space use and sexual fidelity in the field. We find that trade-offs between the benefits of male fidelity and infidelity are reflected in patterns of territorial intrusion, offspring paternity,avprlaexpression, and the evolutionary fitness of alternativeavprlaalleles. DNA variation at theavprlalocus includes polymorphisms that reliably predict the epigenetic status and neural expression ofavprla,and patterns of DNA diversity demonstrate thatavprlaregulatory variation has been favored by selection. In prairie voles, trade-offs in the fitness consequences of social behaviors seem to promote neuronal and molecular diversity.