The mirror system, comprising cortical areas that allow the actions of others to be represented in the observer’s own motor system, is thought to be crucial for the development of social cognition in humans. Despite the importance of the human mirror system, little is known about its origins. We investigated the role of sensorimotor experience in the development of the mirror system. Functional magnetic resonance imaging was used to measure neural responses to observed hand and foot actions following one of two types of training. During training, participants in the Compatible (control) group made mirror responses to observed actions (hand responses were made to hand stimuli and foot responses to foot stimuli), whereas the Incompatible group made counter-mirror responses (hand to foot and foot to hand). Comparison of these groups revealed that, after training to respond in a counter-mirror fashion, the relative action observation properties of the mirror system were reversed; areas that showed greater responses to observation of hand actions in the Compatible group responded more strongly to observation of foot actions in the Incompatible group. These results suggest that, rather than being innate or the product of unimodal visual or motor experience, the mirror properties of the mirror system are acquired through sensorimotor learning.