Demetrius first appears in the charter dated to 1413. Traditional Georgian historiography founded by Prince Vakhushti in the 18th century erroneously makes him a younger brother of George VIII and frequently omits him from the list of the kings of Georgia. Demetrius was co-opted by his father Alexander I in 1433. He was sent by him as ambassador to Shah Rukh, Timur's son.^[1]

After Alexander I's renouncement of the throne in 1442 in favor of Vakhtang IV, Demetrius remained a co-king with the latter, whereas Alexander's third son, George VIII, was made a co-king appanaged in Kakheti. Upon the death of Vakhtang IV in 1446, Demetrius III was to become de jure king-regnant of Georgia, but the throne was seized by George VIII, inaugurating a series of conflicts which would eventually lead to the dissolution of the kingdom of Georgia by the close of the 15th century. Demetrius retired to the western province of Imereti. He was killed by a horse while hunting in 1453.^[1]

Demetrius was married, sometime after 1446, to Gulashar, whom Marie-Félicité Brosset identified with his aunt Gulkan, the widow of Demetrius's paternal uncle George. She died in 1471 or c. 1475. Their son, Constantine II, was the last king of a united Georgia (1478–1490) and the first king of Kartli (1490–1505).^[1]

The historian Vakhushti claims that Demetrius had another son, David, who was installed as king in Kakheti in 1465 by the local nobility and founded the dynasty of the kings of Kakheti. Vakhushti makes David the father of George, king of Kakheti, whom he differentiates from George VIII, Demetrius's younger brother, at first king of Georgia and then king of Kakheti. The David of Vakhushti is, however, a fictitious figure.^[2]

• Toumanoff, Cyril (1949–51). "The Fifteenth-Century Bagratids and the Institution of Collegial Sovereignty in Georgia". Traditio. 7: 169–221. doi:10.1017/S0362152900015142. S2CID 149043757.