Andronikos was born during the reign of his grandfather, Andronikos II, to Michael IX and Rita of Armenia. He was disinherited by his grandfather following the accidental murder of Manouel, the junior Andronikos's younger brother, on the younger Andronikos's orders, though he meant only to kill his mistress's lover, and did not realise that the man in question was his brother. The death of Manouel is said to have caused the death of their father, Michael IX, through grief. Raising an army to challenge his grandfather, between 1321 and 1328 the grandfather and grandson engaged in a civil war which resulted in the forced abdication of the grandfather.

The monetary economy of the Byzantine Empire continued its transition to a silver-based bimetallic system, but does include some enigmatic undatable heavily debased gold coins. These contain on the obverse a depiction of Andronikos kneeling before Christ, and on the reverse Anna of Savoy, Andronikos's wife, and their son, John V. It is unclear whether these coins belong to the reign of Andronikos III, promoting his son and heir on the coins, or whether they belong to the period of Anna's regency for John during the civil war that ensued following Andronikos's death in 1341. If the latter, then Andronikos was the first deceased emperor to be portrayed on coins since the appearance of Michael II on the coins of Theophilos in the 830s (discounting Constantine I, who appears as Saint Constantine as much as if not more than as a deceased emperor).

After Andronikos's premature death in 1341, his 9-year-old son, John, was left as emperor. Andronikos designated his close friend and ally, John Kantakouzenos, as head of the government, but the distrust between him and Anna led to a second Palaiologan civil war.

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