The tendency to trust and to cooperate increases from adolescence to adulthood. This social development has been associated with improved mentalizing and age-related changes in brain function. Thus far, there is limited imaging data investigating these associations. We used two trust games with a trustworthy and an unfair partner to explore the brain mechanisms underlying trust and cooperation in subjects ranging from adolescence to mid-adulthood. Increasing age was associated with higher trust at the onset of social interactions, increased levels of trust during interactions with a trustworthy partner and a stronger decline in trust during interactions with an unfair partner. Our findings demonstrate a behavioural shift towards higher trust and an age-related increase in the sensitivity to others' negative social signals. Increased brain activation in mentalizing regions, i.e. temporo-parietal junction, posterior cingulate and precuneus, supported the behavioural change. Additionally, age was associated with reduced activation in the reward-related orbitofrontal cortex and caudate nucleus during interactions with a trustworthy partner, possibly reflecting stronger expectations of trustworthiness. During unfair interactions, age-related increases in anterior cingulate activation, an area implicated in conflict monitoring, may mirror the necessity to inhibit pro-social tendencies in the face of the partner's actual levels of cooperation. © The Author (2012). Published by Oxford University Press.