Ay was born a commoner, probably at Akhmim, the city the Greeks called Panopolis, in the ninth nome of Upper Egypt. He may have been the son of Yuya and Tjuyu, the wealthy provincial couple whose magnificent tomb in the Valley of the Kings proved they had risen to the highest circles of power, which would make him the brother of Tiye, the Great Royal Wife of Amenhotep III, the magnificent pharaoh who ruled Egypt at the zenith of its wealth and built Luxor Temple and the Colossi of Memnon. Whether this relationship is true or merely circumstantial, Ay certainly came from the same town and held the same titles as Yuya: God's Father and Master of Horses. He began his career in the army, rising through the ranks from troop commander to Overseer of All the Horses of His Majesty, the highest position in the elite chariot corps, just below the rank of general. From there he became Fan-bearer on the Right Side of the King, a ceremonial title that meant he stood at the pharaoh's right hand and had the king's ear.

By the time Akhenaten moved the capital from Thebes to a new desert city called Akhetaten, the Horizon of the Aten, Ay was already one of the most powerful men in the kingdom. The Aten was the sun disk, a solar orb whose rays ended in tiny hands that pressed the ankh, the key of life, to the noses of the king and queen, and Akhenaten declared it the only god worthy of worship, closing the temples of Amun and every other deity in Egypt. Ay built himself a rock-cut tomb at Amarna, Southern Tomb 25, and had the Great Hymn to the Aten inscribed on its walls, the same hymn that celebrated the sun disk as the sole creator of all life. Whether he believed in the new religion or merely survived it, he navigated the heretic's court with the skill of a man who understood that power flows to those who stand closest to the throne.

When Akhenaten died and the boy Tutankhamun ascended the throne at nine or ten years old, Ay became the guiding hand behind the restoration of the old gods. The Amun priesthood, whose power had been stripped away by Akhenaten, returned to prominence, and the capital moved back to Thebes. Tutankhamun reigned for approximately nine years, and for most of that time Ay served as his chief advisor, possibly as vizier, though the title is not definitively attested. Some Egyptologists, including Bob Brier, have suggested that Ay murdered the boy king to seize the throne, a theory based on X-ray examinations of Tutankhamun's mummy conducted in 1968, though subsequent CT scans in 2005 found no evidence of a fatal blow to the head. The cause of Tutankhamun's death remains one of Egyptology's open questions.

What is certain is that Ay moved swiftly. Tutankhamun died without an heir, and the Commander of the Army, Horemheb, had been designated as the Deputy of the Lord of the Two Lands, the heir apparent. But Ay outmanoeuvred him. He married Ankhesenamun, Tutankhamun's widow and the daughter of Akhenaten and Nefertiti, the most beautiful queen Egypt had ever known, a union that connected him by marriage to the royal bloodline. Then he performed the Opening of the Mouth ceremony on Tutankhamun's mummy, a ritual in which a priest touched the eyes, mouth, and nostrils of the dead with special implements to restore their senses for the afterlife. The wall painting in Tutankhamun's burial chamber, KV62, depicts Ay wearing the blue war crown and performing this rite, an explicit claim of succession that no Egyptian artist had ever rendered so boldly. The message was clear: the commoner was now king.

Ay adopted the full royal titulary. His praenomen was Kheperkheperure, Everlasting are the Manifestations of Re, the supreme sun god whose barque crossed the heavens each day, and his Horus name was Kanakhte-Tjehenkhau, Strong Bull of Glittering Crowns. He reigned for only four years, probably from 1323 to 1319 BCE, already an old man when he took the throne. He continued the restoration of traditional religion, adding his own inscriptions beside those of Tutankhamun at Luxor Temple and building a mortuary temple at Medinet Habu on the west bank of Thebes. He designated two men as Hereditary Prince during his reign: Nay, his chief palace official, and Nakhtmin, a general who was probably his son or adopted son. A dyad statue of Nakhtmin and his wife bears the titles Crown Prince and King's Son, proof that Ay intended Nakhtmin to succeed him.

But Ay's plans died with him. When he passed away of natural causes, Horemheb seized the throne and became the last pharaoh of the Eighteenth Dynasty. Then he set about erasing Ay from history. Horemheb usurped Ay's mortuary temple at Medinet Habu, carving his own name over Ay's inscriptions. He desecrated Ay's tomb, WV23 in the Western Valley of the Kings, smashing the sarcophagus into pieces and cutting the cartouches from the walls. The tomb had probably been begun for Tutankhamun and reassigned to Ay when the boy king died suddenly, and now Horemheb made sure that even the stone would forget the commoner who had dared to become pharaoh. Only one cartouche escaped the chisel, buried under debris, and it was not discovered until 1972 when the archaeologist Otto Schaden found the intact sarcophagus lid hidden in the rubble.

Ay was not merely erased by Horemheb. He was erased by time itself. The Amarna Period, that brief experiment in monotheism that had shaken Egypt to its foundations, became a memory that later pharaohs preferred to forget. Akhenaten was called the criminal, the heretic, and his successors systematically destroyed his city, his name, and his god. Ay, who had served the heretic and then profited from his fall, was caught in the same net of damnatio memoriae, the Roman term for the condemnation of memory that the Egyptians practised long before the Romans gave it a name. Yet the wall painting in Tutankhamun's tomb survived, and the sarcophagus lid survived, and the Great Hymn to the Aten in Ay's Amarna tomb survived, fragments of a life that refused to be entirely erased.