Studies demonstrating selective brain networks subserving motivation and mentalization (i.e. attributing states of mind to others) during social interactions have not investigated their mutual independence. We report the results of two fMRI studies using a competitive game requiring players to use implicit ‘on-line’ mentalization simultaneously with motivational processes of gains and losses in playing against a human or a computer opponent. We delineate a network, consisting of bilateral temporoparietal junction, temporal pole (TP), medial prefrontal cortex (MPFC) and right fusiform gyrus, which is sensitive to the opponent’s response (challenging>not challenging the player) and opponent type (human>computer). This network is similar to a known explicit ‘off-line’ mentalization circuit, suggesting its additional involvement in implicit ‘on-line’ mentalization, a process more applicable to real-life social interactions. Importantly, only MPFC and TP were selective to mentalization compared to motivation, highlighting their specific operation in attributing states of mind to others during social interactions.