Aglaurus was born in the earliest days of Attica, when the land was called Acte or Actaea after her father Actaeus, the first king of what would one day become Athens. Actaeus was an autochthon, one of the "sons of the soil" who had no father or mother but rose directly from the earth, and his name spoke of the coast he ruled. Some say a man named Colaenis ruled before him, but most traditions give Actaeus the honour of being the first to hold sway over the rocky peninsula of Attica. He fathered at least one daughter, Aglaurus, and possibly more, though the ancient sources disagree on whether Herse and Pandrosos were also daughters of Actaeus or whether they were born later to Aglaurus herself.

When Aglaurus came of age, her father gave her in marriage to Cecrops, another autochthon who had emerged from the soil of Attica with a body that was human above the waist and serpentine below. Cecrops was a figure of primal wisdom, the first to establish marriage among the Athenians, to divide Attica into twelve communities, and to abolish the bloody sacrifice of living creatures to Zeus in favour of offering sacred cakes called pelanoi. Through his marriage to Aglaurus, Cecrops inherited the throne of Acte and renamed the land Cecropia after himself. The marriage was thus not merely a union of two people but a transfer of sovereignty, the moment when the old coast kingdom passed into the hands of the serpent-king who would found a civilisation.

Aglaurus bore Cecrops at least four children. Their only son was Erysichthon, a prince who predeceased his father and died without children, leaving the kingdom without a male heir. Their three daughters were Aglaurus, named for her mother; Herse, whose name means "dew"; and Pandrosos, whose name means "all-dewy." These three girls, the Cecropids, would become central to one of Athens' most sacred myths. When Athena, the goddess of wisdom and warfare, entrusted the infant Erichthonius to their care in a sealed chest, it was the daughters of Aglaurus who received him. Two of them - the eldest Aglaurus and Herse - opened the forbidden chest and were driven mad by the sight of the serpent-child within, leaping to their deaths from the Acropolis. Only Pandrosos obeyed, and she was rewarded with a sanctuary on the sacred hill. Aglaurus the mother thus saw two of her daughters destroyed by divine punishment and one honoured by divine favour, a mother's grief and pride intertwined in the very foundation myth of the city.

The most famous event of Cecrops' reign - and therefore of Aglaurus' life as queen - was the contest between Athena and Poseidon for the patronage of Athens. Poseidon struck the rock of the Acropolis with his trident and produced a saltwater spring, or in some tellings a horse, as his gift to the city. Athena planted an olive tree on the same rock, a symbol of peace and prosperity that would feed the people for generations. The twelve gods of Olympus were appointed as judges, and Cecrops was called upon as a witness. He testified that Athena had been the first to plant her tree, and the gods awarded the city to her. Athena named it Athens after herself, and Poseidon in his rage flooded the Thriasian plain. Aglaurus would have stood beside her husband during this cosmic dispute, the queen of a city that had not yet been named, watching the gods themselves compete for the right to protect her husband's kingdom. The olive tree Athena planted was shown to visitors on the Acropolis for a thousand years, and every Athenian who ever swore an oath by it, every soldier who ever wore a crown of olive leaves, owed something to the queen who had witnessed its planting.

Aglaurus' legacy extended far beyond her own lifetime through her descendants. Her daughter Aglaurus, the princess, bore Alcippe to Ares, the god of war, and when that daughter was violated by Halirrhothius, the son of Poseidon, Ares killed the rapist and was tried before the gods on the Areopagus, the Hill of Ares. That trial established the court as the seat of Athenian justice. Through Herse, Aglaurus became the grandmother of Cephalus, the hunter whose story would be told by Ovid. Through Pandrosos, she became the ancestress of the priestly families who tended the oldest shrines on the Acropolis. And through her husband Cecrops, she was connected to the entire autochthonous line of Athenian kings that ran from the earth itself through Erichthonius and Erechtheus to Aegeus and finally to Theseus, the hero who slew the Minotaur in Crete.