Erichthonius was born in Athens, or rather beneath it, in the smithy of Hephaestus on the Acropolis itself. Hephaestus, the god of fire and metalworking, had fallen in love with Athena, the virgin goddess of wisdom and war, and had tried to force himself upon her. Athena, the daughter of Zeus who had sprung fully armed from her father's forehead, was not a goddess who submitted to any male, divine or mortal. She fought Hephaestus off, and in the struggle his seed fell upon the earth, upon Gaia, the primordial mother whose body was the soil of Greece itself. Gaia received the seed and brought forth a child, a boy who was half-human and half-serpent, his lower body coiled like a snake, his upper body the image of a divine infant. He was autochthonous, born from the chthon, the earth, with no mortal mother to claim him, and in this he was the perfect symbol of Athens, the city that prided itself on being the oldest in Greece because its people had always lived on the same soil.

Athena took pity on the child, or perhaps she recognised in him a weapon against those who would question her virginity. She placed the infant in a small chest or casket, a larnax of woven wicker, and set a serpent to coil around him as his guardian. Then she carried the chest to the daughters of Cecrops, the first king of Athens, a man who was himself half-serpent, born from the autochthonous soil of Attica before the flood. Cecrops had three daughters, Aglaurus, Herse, and Pandrosus, and Athena entrusted the chest to them with a solemn command: they must not open it. They must not look inside. They must guard it with their lives and tell no one what it contained. The daughters agreed, and Athena departed, leaving the chest in their keeping on the Acropolis, in the shadow of her own temple.

The daughters of Cecrops could not resist. Curiosity, or perhaps divine compulsion, drove them to lift the lid of the chest and peer inside. What they saw drove them mad. Some accounts say they saw the infant Erichthonius with the serpent coiled around him, a sight so terrible that their minds broke. Other accounts say that Athena had set two additional serpents inside the chest as guardians, and the girls were bitten and died. In the most common version, Aglaurus and Herse were driven mad by the sight and threw themselves from the Acropolis, falling to their deaths on the rocks below, while Pandrosus, the youngest, either survived or was turned to stone for her part in the transgression. The serpent that guarded Erichthonius survived, and Athena took the child back and raised him herself, or gave him to the wife of Cecrops to nurse in secret.

When Erichthonius grew to manhood, he became king of Athens, succeeding Cecrops or his successor Cranaus, depending on which king-list one follows. His reign was prosperous and innovative. He invented the chariot, not merely as a vehicle of war but as a means of concealing his serpentine lower body from the gaze of mortals, who might have been driven mad by the sight of his true form as the daughters of Cecrops had been. He harnessed four horses to his chariot and rode through the streets of Athens in state, the first king to do so, and the chariot became the symbol of Athenian royalty. He also founded the Panathenaea, the great festival in honour of Athena that was celebrated every four years with athletic contests, musical competitions, and a sacred procession along the Panathenaic Way to the Acropolis, where a new robe was presented to the goddess's ancient wooden statue.

Erichthonius was buried in Athens, a singular honour. Most Greek cities forbade burial within the walls, fearing pollution, but Erichthonius was autochthonous, born from the earth of the Acropolis, and it was fitting that he should return to it. His tomb lay within the precinct of the temple of Athena Polias, the most sacred spot on the Acropolis, and his serpent guardian continued to dwell there, receiving offerings of honey cakes from the priests. When the Erechtheion was built in the fifth century BCE, the temple incorporated both his tomb and the sacred serpent, and the name of Erichthonius was gradually conflated with that of his descendant Erechtheus, a later king who fought a war against Eleusis and was killed by Poseidon's trident. The two names became one in Athenian cult, and the Erechtheion housed the shrines of both, along with the wooden statue of Athena that Erichthonius himself was said to have dedicated.