Aethra was born in Troezen, a city on the eastern coast of the Peloponnese, the daughter of King Pittheus and granddaughter of Pelops, the legendary king of Pisa in Elis whose chariot race won him a bride and whose descendants shaped the history of Greece. She grew up in her father's palace, a princess of ancient lineage, and for a time she was courted by Bellerophon, the hero who would later tame the winged horse Pegasus and slay the Chimera, the fire-breathing monster, but Bellerophon was exiled for killing a kinsman before the marriage could take place. Her life changed when Aegeus, the king of Athens, arrived at Troezen. Aegeus had visited the oracle at Delphi to ask how he might father an heir, and the priestess had answered him in a riddle: "Loose not the bulging mouth of the wineskin until you have reached the height of Athens." Aegeus did not understand, but Pittheus did. He plied the Athenian king with wine and led him to Aethra's bed.

That same night, the goddess Athena sent Aethra a dream. She instructed the princess to wade across the narrow channel to the island of Sphaeria, which lay just off the coast of Troezen, and there pour a libation to the spirit of her grandfather's charioteer. Aethra rose and did as she was told, wading through the dark water to the island. But as she made her offering, Poseidon, the god of the sea, rose from the waves and lay with her. When Aegeus awoke and learned that Aethra was with child, he placed his sword and a pair of sandals beneath a great rock that served as an altar to Zeus the Strong, and told her that if she bore a son who could lift the stone, she should send him to Athens with the tokens as proof of his royal birth. Then he returned to Athens, and Aethra gave birth to a boy she named Theseus, a child who would claim descent from both a king and a god.

For years Aethra raised her son in Troezen under the guidance of her father Pittheus, and when Theseus came of age she led him to the great rock and showed him what lay beneath it. The boy lifted the stone with ease, retrieved the sword and sandals, and set out for Athens by the overland road, determined to prove himself a hero before claiming his birthright. Aethra remained in Troezen, and later she bore a daughter named Clymene, half-sister to Theseus, who would share in the trials to come. But Aethra's own trials were only beginning. Theseus, now king of Athens, and his friend Pirithous, king of the Lapiths, a tribe from Thessaly, conceived a mad plan to marry daughters of Zeus. They kidnapped Helen, the young daughter of Tyndareus of Sparta, the most beautiful woman ever born, and Theseus entrusted her to his mother's care at Aphidna, one of the twelve ancient towns of Attica, the region ruled by Athens.

While Theseus and Pirithous descended to the underworld in their attempt to seize Persephone, the queen of the dead and wife of Hades, Helen's twin brothers Castor and Polydeuces, known together as the Dioscuri, marched on Aphidna with a Spartan army. They stormed the town, rescued Helen, and took Aethra and her daughter Clymene as captives back to Sparta. There Aethra became Helen's slave, a princess of Troezen reduced to servitude in a foreign land. When Helen later married Menelaus, the king of Sparta, and then eloped with Paris, the Trojan prince, to Troy, Aethra accompanied her, crossing the sea to the city that would become the grave of a generation. In Troy she served Helen faithfully, and in some accounts she helped raise her great-grandson Munitus, the son of her grandson Acamas and Laodice, a daughter of King Priam. For ten years she lived in the besieged city, an old woman watching the war from within the walls.

When Troy finally fell to the Greeks, Aethra made her way to the Greek camp with shaven head and mourning dress, and there she was recognised by her grandsons Acamas and Demophon, the sons of Theseus. They pleaded with Agamemnon, the high king of the Greek forces, to secure her freedom, and Agamemnon sent a messenger to Helen to ask that the old woman be released. Helen, who had known Aethra's kindness in Sparta and Troy, granted the request. Aethra and Clymene were freed and returned to Athens in triumph, escorted by Menestheus, the leader of the Athenians at Troy. According to the mythographer Hyginus, Aethra later took her own life from grief at the death of her sons, though other accounts let her live out her days in the city her son had made great. Her story was carved upon the chest of Cypselus at Olympia and painted by Polygnotus in the Lesche at Delphi, a life that had touched the edges of every great legend of the age.