Parthenopaeus was the son of Atalanta, his father given variously as her husband Melanion, the hero Meleager, or the god Ares. A less common version instead makes him a son of Talaus and Lysimache.

According to Hyginus, Atalanta left the infant exposed on Mount Parthenius in Arcadia so as to conceal the fact that she was no longer a virgin. He was rescued by a shepherd and reared alongside Telephus, with whom he became a close companion. The two later joined in defending the kingdom of Teuthras (Teuthrania), helping to repel an invasion. Euripides records that Parthenopaeus moved to Argos as a young man, where he was given a friendly reception.

Parthenopaeus was persuaded by Adrastus to join the expedition of the Seven against Thebes. He was assigned to assault one of the city's gates, named in the sources as either the Electran or the Neitian Gate.

In Aeschylus's account he bore a shield emblazoned with the Sphinx clutching a Theban victim, and he swore by his spear to sack the city. He was killed at the wall, the slayer being given differently as Periclymenus or Amphidicus; according to Euripides, Periclymenus crushed his head by hurling a stone down upon him. Statius's Thebaid gives an extended description of his fierce fighting and death, and his shade is also evoked in Virgil's Aeneid.

Parthenopaeus left a son who took part in the Epigoni, the expedition of the sons of the Seven that succeeded in taking Thebes. This son is most often named Promachus, though some traditions instead call him Tlesimenes or Stratolaus, and name his mother as the nymph Clymene.