In constructing improved models of human behavior, both experimental and behavioral economists have increasingly turned to evolutionary theory for insights into human psychology and preferences. Unfortunately, the existing genetic evolutionary approaches can explain neither the degree of prosociality (altruism and altruistic punishment) observed in humans, nor the patterns of variation in these behaviors across different behavioral domains and social groups. Ongoing misunderstandings about why certain models work, what they predict, and what the place is of “group selection” in evolutionary theory have hampered the use of insights from biology and anthropology. This paper clarifies some of these issues and proposes an approach to the evolution of prosociality rooted in the interaction between cultural and genetic transmission. I explain how, in contrast to non-cultural species, the details of our evolved cultural learning capacities (e.g., imitative abilities) create the conditions for the cultural evolution of prosociality. By producing multiple behavioral equilibria, including group-beneficial equilibria, cultural evolution endogenously generates a mechanism of equilibrium selection that can favor prosociality. Finally, in the novel social environments left in the wake of these cultural evolutionary processes, natural selection is likely to favor prosocial genes that would not be expected in a purely genetic approach.