According to a passage considered to be an interpolation in the history of Laonikos Chalkokondyles, he accused his mother Theodora of having an affair with an unnamed protovestiarios, whom he killed, then held his parents captive in the citadel until the palace staff released them.

[7] In February 1451 the Byzantine diplomat George Sphrantzes arrived in Trebizond seeking a bride for his emperor, Constantine XI Palaiologos.

Mehmed II immediately summoned John to pay tribute in Constantinople and imposed heavy tolls on Trapezuntine and Venetian shipping through the straits.

John apparently failed to cooperate, and in 1456 the Sultan dispatched his governor of Amasya Hizir Bey to attack Trebizond by both land and sea.

As early as 1434 he had responded to the letters of Pope Eugenius IV, in marked contrast to earlier emperors of Trebizond, who had ignored papal missives.

[13] John's hostile attitude towards Genoa was explained by one contemporary, the Spanish traveller Pero Tafur, as a fear of a potential Byzantine-Genoese alliance that could place his brother Alexander on the throne of Trebizond.

Alexander had fled Trebizond for the Byzantine court in 1429 and had eventually married Maria Gattilusio, the daughter of the Genoese lord of Lesbos.

[14] At some point in his reign, John was faced with an attack by the ruler of Ardabil, Shaykh Junayd, who marched upon Trebziond: proposed dates range from the 1430s (E. Janssens) through the 1440s (von Hammer, Finlay, and Miller) to 1456 (Shukurov) or 1456-58 (Anthony Bryer).

[16] Beginning with Jakob Philipp Fallmerayer, modern scholars have inferred it from two records: one was a letter from John's successor and brother, David of Trebizond, dated 22 April 1459, but because it was associated with the dubious embassy led by Ludovico da Bologna, and internal inconsistencies, this letter has been considered at the least a partial forgery; the other record was a damaged inscription Fallmerayer reported to have seen in the citadel Kule boylu ("high tower"), which was made by John and dated to the year 6968 (= A.D. 1 September 1459 – 31 August 1460); however this inscription was never seen by any other historian, despite determined efforts, and the citadel itself has since been destroyed.

Since William Miller wrote his book on Trebizond, the scholarly consensus dated his death to 1458, although with some dissent to 1459 (Lampsides, Kursanskis) or simply state the broad limits 1458/9-1460 (Anthony Bryer).

Once these two sources are accepted as plausible, then there is no longer any basis to reject the evidence of the lost inscription Fallmerayer reported seeing on the Kule boylu.

[19] However, researchers from Kuršanskis in 1979 onwards consider it likely that John had only one child—Theodora Megale Komnene, better known by her Mongol appellation "Despina Hatun" (who married Uzun Hassan).

Valenza, wife of Nicholas Crispo, Lord of Syros, was called a sister of Theodora by Giovanni Battista Ramusio, but this appears to be an error.