It has been suggested that the human species may be undergoing an evolutionary transition in individuality (ETI). But there is disagreement about how to apply the ETI framework to our species, and whether culture is implicated as either cause or consequence. Long-term gene–culture coevolution (GCC) is also poorly understood. Some have argued that culture steers human evolution, while others proposed that genes hold culture on a leash. We review the literature and evidence on long-term GCC in humans and find a set of common themes. First, culture appears to hold greater adaptive potential than genetic inheritance and is probably driving human evolution. The evolutionary impact of culture occurs mainly through culturally organized groups, which have come to dominate human affairs in recent millennia. Second, the role of culture appears to be growing, increasingly bypassing genetic evolution and weakening genetic adaptive potential. Taken together, these findings suggest that human long-term GCC is characterized by an evolutionary transition in inheritance (from genes to culture) which entails a transition in individuality (from genetic individual to cultural group). Thus, research on GCC should focus on the possibility of an ongoing transition in the human inheritance system.