Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food–giving behaviour motivated the design of experiments 2–4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by–product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.