Stefan I Crnojević consolidated his power in Zeta and ruled for 14 years, from 1451 until 1465. During his rule, he saw the Despotate completely subdued by the Ottomans soon after the death of Despot Đurađ Branković. Under Stefan Crnojević, Zeta comprised the Lovćen area around Cetinje, 51 municipalities which included the Crnojević River, the Zeta valley, and the tribes of Bjelopavlići, Pješivci, Malonšići, Piperi, Hoti, Kelmendi and others. The population of the territories controlled by Stefan was ca. 30,000, while the total population of the Zeta region (including territories under foreign rule) was ca. 80,000.

Capitalising on the weak position of Despot Đurađ, the Venetians and Herzog Stjepan Vukčić Kosača of St. Sava (the region of Herzegovina is named after him) conquered parts of his territory. Stefan I Crnojević, who had already established himself as the head of the Crnojević (around 1451) in Upper Zeta was forced to make territorial concessions. In addition, Kosača took Stefan's son Ivan as a political hostage, hoping it would force Stefan to side with him whenever needed.

Stefan married Mara, a daughter of a prominent Albanian Gjon Kastrioti, whose son was the Albanian national hero, Skanderbeg. In 1455, Stefan entered into an agreement with his ally Venice, stipulating that Zeta would recognize the nominal supremacy of Venice while maintaining its factual independence in virtually every respect. The agreement also stipulated that Zeta would assist Venice militarily on specific occasions in exchange for an annual provision. But in all other respects, Stefan's rule in Zeta was undisputed.