Culture suffuses all aspects of human life. It shapes our minds and bodies and has provided a cumulative inheritance of knowledge, skills, institutions, and artifacts that allows us to truly stand on the shoulders of giants. No other species approaches the extent, diversity, and complexity of human culture, but we remain unsure how this came to be. The very uniqueness of human culture is both a puzzle and a problem. It is puzzling as to why more species have not adopted this manifestly beneficial strategy and problematic because the comparative methods of evolutionary biology are ill suited to explain unique events. Here, we develop a more particularistic and mechanistic evolutionary neuroscience approach to cumulative culture, taking into account experimental, developmental, comparative, and archaeological evidence. This approach reconciles currently competing accounts of the origins of human culture and develops the concept of a uniquely human technological niche rooted in a shared primate heritage of visuomotor coordination and dexterous manipulation.