Son of King David VII and his wife Gvantsa, Demetrius was only 2 years old when his mother was killed by the Mongols in 1261. He succeeded on his father's death in 1270, when he was 11 years old. He ruled under the regency of Sadun Mankaberdeli for some time. In 1277–1281, he took part in Abaqa Khan's campaigns against Egypt and in particularly distinguished himself at the Second Battle of Homs, (29 October 1281). Although he continued to be titled "king of Georgians and Abkhazians, etc", Demetrius’s rule extended only over the eastern part of the kingdom. Western Georgia was under the rule of the Imeretian branch of the Bagrationi dynasty.

King Demetrius was considered quite a controversial person. Devoted to Christianity, he was criticized for his polygamy.[citation needed] In 1288, on the order of Arghun Khan, he subdued the rebel province of Derbend at the Caspian Sea. The same year, Arghun revealed a plot organized by his powerful minister Buqa, whose son was married to Demetrius's daughter. Bugha and his family were massacred, and the Georgian king, suspected to be involved in a plot, was ordered to the Mongol capital, or Arghun threatened to invade Georgia. Despite much advice from nobles, Demetrius headed for the Khan’s residence to face apparent death, and was imprisoned there. He was beheaded at Movakan on 12 March 1289. He was buried at Mtskheta, Georgia, and canonized by the Georgian Orthodox Church.

He was succeeded by his cousin Vakhtang II.