The Caucasus and surrounding areas, with their rich metal resources, became a crucible of the Bronze Age1 and the birthplace of the earliest steppe pastoralist societies2. Yet, despite this region having a large influence on the subsequent development of Europe and Asia, questions remain regarding its hunter-gatherer past and its formation of expansionist mobile steppe societies3-5. Here we present new genome-wide data for 131 individuals from 38 archaeological sites spanning 6,000 years. We find a strong genetic differentiation between populations north and south of the Caucasus mountains during the Mesolithic, with Eastern hunter-gatherer ancestry4,6 in the north, and a distinct Caucasus hunter-gatherer ancestry7 with increasing East Anatolian farmer admixture in the south. During the subsequent Eneolithic period, we observe the formation of the characteristic West Eurasian steppe ancestry and heightened interaction between the mountain and steppe regions, facilitated by technological developments of the Maykop cultural complex8. By contrast, the peak of pastoralist activities and territorial expansions during the Early and Middle Bronze Age is characterized by long-term genetic stability. The Late Bronze Age marks another period of gene flow from multiple distinct sources that coincides with a decline of steppe cultures, followed by a transformation and absorption of the steppe ancestry into highland populations.