Dvin was founded by the Armenian king Khosrov III Kotak (r. c. 330 - 338 CE) who converted what was already a small settlement and royal hunting park into a new city. The ancient city of Dvin was built by Khosrov III Kotak in 335 on a site of an ancient settlement and fortress from the 3rd millennium BC. Since then, the city had been used as the primary residence of the Armenian Kings of the Arsacid dynasty. Dvin boasted a population of about 100,000 citizens in various professions, including arts and crafts, trade, fishing, etc. 

After the fall of the Armenian Kingdom in 428, Dvin became the residence of Sassanid appointed marzpans (governors), Byzantine kouropalates and later Umayyad- and Abbasid-appointed ostikans (governors). Under Arsacid rule, Dvin prospered as one of the most populous and wealthiest cities east of Constantinople. Its prosperity continued even after the partition of Armenia between Romans and Sassanid Persians, when it became the provincial capital of Persian Armenia, and eventually it became a target during the height of the Early Muslim conquests. According to Sebeos and Catholicos John V the Historian, Dvin was captured by the Arabs in 640 during the reign of Constans II and Catholicos Ezra. During the Arab conquest of Armenia, Dvin was captured and pillaged in 640, in the first raids. On January 6, 642 the Arabs stormed and took the city, with many deaths. Dvin became the center of the Muslim province of Arminiya, the Arabs called the city Dabil.

Although Armenia was a battleground between Arabs and Byzantine forces for the next two centuries, in the 9th century it still flourished. Frequent earthquakes and continued warfare led to the decline of the city from the beginning of the 10th century. During a major earthquake in 893, the city was destroyed, along with most of its 70,000 inhabitants.