Aglaurus was born to Cecrops, the autochthonous king who rose from the soil of Attica with the body of a serpent below the waist and the torso of a man above it, and to Agraulus, the daughter of Actaeus, the even earlier king of the land. She had two sisters, Herse and Pandrosos, and together the three were called the Cecropids or the Kekropidai, the daughters of the snake-king. Their brother Erysichthon died without children, and so the royal line of Athens passed not through sons but through the daughters of Cecrops, making Aglaurus and her sisters the ancestresses of the city's greatest heroes. Aglaurus herself caught the eye of Ares, the Olympian god of war and bloodshed, and by him she bore a daughter named Alcippe, a princess of divine and royal blood.

The first great drama of Aglaurus' life involved her daughter. Alcippe grew to be a maiden of extraordinary beauty, and one day as she walked near the shore she was seized and violated by Halirrhothius, the son of Poseidon, the god of the sea. Ares discovered the crime and struck Halirrhothius down with a single blow of his spear. Poseidon demanded justice for the murder of his son and brought Ares before the twelve gods on a rocky hill west of the Acropolis. The gods acquitted Ares, ruling that a father who kills his daughter's rapist has committed no crime, and from that day the hill was called the Areopagus, the Hill of Ares, and became the seat of Athens' most ancient and solemn court. Aglaurus watched this trial from the palace, her daughter's honour defended by divine law and her own name forever linked to the birthplace of Athenian justice.

But Aglaurus is remembered less for her daughter than for the chest. When Hephaestus, the lame smith-god of the forge, tried to force himself upon Athena and spilled his seed upon the earth instead, the soil of the Acropolis conceived a child. Gaia, the primordial Earth, brought forth Erichthonius, a boy whose lower half was formed like a serpent. Athena took the infant into her care, hid him in a wicker chest, and entrusted the chest to the three daughters of Cecrops with a single command: do not open it. Pandrosos, the youngest sister, obeyed. But Aglaurus and Herse could not resist. They lifted the lid and looked inside. Some say they saw the infant guarded by a pair of serpents. Others say they saw the child himself in his serpent form. Athena, returning from Pellene where she had gone to fetch a mountain to fortify the citadel, learned from a crow what had happened. In her fury she drove the two disobedient sisters mad. Aglaurus and Herse fled shrieking across the Acropolis and threw themselves from its northern cliff, falling to their deaths on the rocks below. Pandrosos alone was spared, and Athena made her the nurturer of Erichthonius, who would grow up to become the second king of Athens.

In another telling, preserved by the Roman poet Ovid, Aglaurus survived the chest and lived to commit a second offence against the gods. Hermes, the messenger god with the winged sandals and the caduceus, fell in love with Herse, the youngest and most beautiful of the Cecropid sisters. He came to the house of Cecrops in a cloud of golden light, but Aglaurus barred the door. She demanded gold for entry, or in some versions she was simply eaten by jealousy that her younger sister had attracted a god while she had not. Hermes tried to reason with her, then commanded her to stand aside, but Aglaurus refused. The god touched her with his staff, and in an instant her limbs grew rigid, her blood turned to stone, and she became a dark statue seated before the door she had guarded. Ovid adds a telling detail: her mind had stained the stone black, so that even in her petrified form she bore the mark of her envy.

Despite these stories of disobedience and greed, the Athenians honoured Aglaurus as a heroine. On the northern slope of the Acropolis, near the very cliff from which she had leaped, stood the Aglaurion, her sacred shrine. Every year the city celebrated the Aglauria in her memory. More importantly, every young Athenian man about to begin his military service swore his oath of allegiance not only to Zeus and to Athena but to Aglaurus herself, calling upon her as a guardian of the city. Some said this honour came from a different legend entirely: that when Athens was besieged by the Eleusinians, an oracle declared that the city could only be saved if a noble virgin sacrificed herself. Aglaurus climbed the walls and leaped to her death, and the enemy withdrew in awe. Whether she died for curiosity, for jealousy, or for patriotism, the Athenians never forgot her. Her name was carved into the stones of the Acropolis, and her shrine stood until the last days of pagan Athens.