Trust and cooperation increase from adolescence to adulthood, but studies on gender differences in this development are rare. We investigated gender and age-related differences in trust and reciprocity and associated neural mechanisms in 43 individuals (16–27 years, 22 male). Participants played two multi-round trust games with a cooperative and an unfair partner. Males showed more basic trust towards unknown others than females. Both genders increased trust during cooperative interactions, with no differences in average trust. Age was unrelated to trust during cooperation. During unfair interactions males decreased their trust more with age than females. ROI analysis showed age-related increases in activation in the temporo-parietal junction (TPJ) and dorsolateral prefrontal cortex (dlPFC) during cooperative investments, and increased age-related caudate activation during both cooperative and unfair repayments. Gender differences in brain activation were only observed during cooperative repayments, with males activating the TPJ more than females, and females activating the caudate more. The findings suggest relatively mature processes of trust and reciprocity in the investigated age range. Gender differences only occur in unfair contexts, becoming more pronounced with age. Largely similar neural activation in males and females and few age effects suggest that similar, mature cognitive strategies are employed.