The use of fire is central to human survival and to the processes of becoming human. The earliest evidence for hominin use of fire dates to more than a million years ago. However, only when fire use became a regular part of human behavioral adaptations could its benefits be fully realized and its evolutionary consequences fully expressed. It remains an open question when the use of fire shifted from occasional and opportunistic to habitual and planned. Understanding the time frame of this 'technological mutation' will help explain aspects of our anatomical evolution and encephalization over the last million years. It will also provide an important perspective on hominin dispersals out of Africa and the colonization of temperate environments, as well as the origins of social developments such as the formation of provisioned base camps. Frequencies of burnt flints from a 16-m-deep sequence of archaeological deposits at Tabun Cave, Israel, together with data from the broader Levantine archaeological record, demonstrate that regular or habitual fire use developed in the region between 350,000–320,000 years ago. While hominins may have used fire occasionally, perhaps opportunistically, for some million years, we argue here that it only became a consistent element in behavioral adaptations during the second part of the Middle Pleistocene.