The territory of modern-day Oni has been inhabited since the Bronze Age. Archaeology revealed the artifacts of Colchian culture, particularly a collection of Colchian coins dating back to the 6th-3rd centuries BC. Oni is first chronicled in the 15th century, though a legend has it that the town was founded by the 2nd BC king Pharnajom of Iberia. Located on the crossroads from Northern Caucasus, Kartli (central Georgia), Imereti (western Georgia) and Lower Rach'a, Oni developed into a typical late medieval commercial and multi-religious town.