Cyrene was born in Thessaly, the rugged northern land of mountains and horses, to Hypseus, the king of the Lapiths, and Chlidanope, a Naiad nymph of the springs. The Lapiths were a people famous for their warlike nature and their disastrous encounters with the gods. Hypseus himself was the son of Peneus, the river god whose waters flowed through the Vale of Tempe, and of Creusa, a daughter of Gaia, the primordial Earth. Cyrene grew up in the glens of Mount Pelion and Mount Pindus, a princess who rejected every expectation of her sex. She did not pace beside the loom. She did not join the merry feasts of her household companions. She did not sleep late. Instead she rose before dawn, took up her bronze-tipped javelin and her sword, and went into the wilds to hunt the beasts that threatened her father's herds. She was a companion of Artemis, the virgin huntress goddess of the wilderness, who gave her two hunting dogs, and with their help she won a prize in the funeral games of Pelias, the old king of Iolcus whose death had been contrived by Medea. Nonnus, the late Greek poet, called her "a deer-chasing second Artemis, the girl lionkiller," and praised her as "a champion in the leafy forest with lionslaying hands."

The defining moment of her life came on the slopes of Mount Pelion. A monstrous lion, one of the great beasts that roamed the Thessalian highlands, broke from the forest and attacked her father's flocks. Most princesses would have fled, or called for men, or hidden behind walls. Cyrene did none of these. She went out alone, unarmed but for her courage and her strength, and she wrestled the lion. She seized the beast, matched her strength against its fury, and killed it. The fight was fierce, the dust rising around them, the roar of the lion echoing across the mountain. And Apollo, the long-haired son of Leto, was watching. He had come to Pelion on some god's errand, or perhaps he had been drawn by the sound of the struggle. He saw the girl, lovely-armed and fearless, bring the king of beasts to the ground, and he fell in love. Not with her beauty alone, though that was great, but with her courage, her wildness, her absolute refusal to be what the world expected her to be.

Apollo wanted her, but he was not certain. A god may desire a mortal, but marriage is a different matter. He went to Chiron, the wise centaur who lived in a cave on Pelion, who had raised Achilles and Jason and who knew the hearts of gods and men. Chiron smiled when Apollo asked his counsel. He told the god that he already knew everything - the number of leaves that would sprout in spring, the grains of sand moved by every wave, the whole course of time itself - and that his question was merely a formality. But if the god wished to hear it, Chiron would speak plainly. Cyrene was fit to be the bride of Apollo. He would carry her across the sea to Libya, the third continent, and there he would make her queen of a city that would bear her name. She would bear him a son, and that son would be raised by the Hours and Gaia on nectar and ambrosia, and he would become Aristaeus, the guardian of flocks, the delight of men, a god in all but name.

Apollo needed no further encouragement. That very day he took Cyrene in his golden chariot and drove across the sky to Libya. Aphrodite, the goddess of love, welcomed them when they arrived, laying her light hand upon the god's chariot and casting modesty over their union. She joined them in marriage, the immortal god and the mortal huntress, and Apollo laid with Cyrene in a chamber of gold. There, on the Hill of Myrtles, he founded the city of Cyrene and made her its queen. The land was rich beyond measure, a garden of Zeus where fruits grew in abundance and flocks grazed without number. Libya herself, the goddess of that broad land, welcomed the new queen into her golden halls and gave her a portion of the earth to rule as her lawful possession.

Cyrene bore Apollo at least two sons. The first was Aristaeus, a child of such promise that Hermes, the messenger god, carried him from his mother's arms to the thrones of the Hours and to Gaia, the Earth herself. They fed the infant nectar and ambrosia, the food and drink of the gods, and made him immortal. He grew up under the care of Chiron in his Pelian cave, learning the arts of the countryside: beekeeping, cheesemaking, olive cultivation, and the care of flocks. The Greeks called him Agreus, the Hunter, and Nomius, the Shepherd, and they worshipped him as a god who protected the harvest and the herds. Her second son by Apollo was Idmon, a seer of such skill that he joined the Argonauts on their quest for the Golden Fleece, though he knew from his own prophecies that he would be killed by a boar before the voyage ended. Some sources add a third son, Autuchus, mentioned by Apollonius of Rhodes. In another tradition, Cyrene also bore a son to Ares, the god of war: Diomedes, the king of Thrace who owned the man-eating mares that Heracles would later steal as one of his twelve labours.

Apollo did not leave Cyrene to age and die. He transformed her into a nymph, granting her a long life so that she could hunt forever in the Libyan wilds. He visited her often, standing beside her on the Hill of Myrtles, lifting her hunting nets and showing her the land that was now hers. The historical Greeks, centuries later, founded a real colony on the same spot, sent by the oracle of Apollo at Delphi from the island of Thera. They named their city Cyrene after the mythic queen, and it became one of the most prosperous Greek cities in Africa, famous for its horses, its silphium, and its philosophers. The myth and the history became inseparable. The colonists believed they were fulfilling Apollo's ancient promise, and the poet Pindar, writing his ninth Pythian Ode for a victor from Cyrene in 474 BCE, made the city's divine origin the centrepiece of his song.