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Anthropogenic and natural divergence processes in crop-wild fruit tree complexes are less studied than in annual crops, especially in the Caucasus, a pivotal region for plant domestication. We investigated anthropogenic and natural divergence processes in apples in the Caucasus from using 26 microsatellite markers amplified on 508 wild and cultivated samples. We found two specific Iranian cultivated populations that were differentiated from Malus domestica, the standard cultivated apple worldwide, suggesting a specific local domestication process in Iran. Some Iranian apple cultivars belonged to the Caucasian wild apple gene pools, indicating that farmers also use local wild apple for cultivation. Substantial wild-crop and crop-crop gene flow were also inferred. We identified seven genetically differentiated populations of wild apples (Malus orientalis) in the Caucasus. Niche modeling indicated that these populations likely resulted from range changes linked to the last glaciation. This study pinpoints Iran as a key region in the evolution and domestication of apple and further demonstrates the role of gene flow during fruit tree domestication as well as the impact of climate change on the natural divergence of a wild fruit tree. The results also provide a practical base for apple conservation and breeding programs in the Caucasus.