Caesarion was born on 23 June 47 BCE in Alexandria, the glittering capital of the Ptolemaic Kingdom that his Greek ancestors had ruled for nearly three centuries. His conception occurred during Julius Caesar's extended stay in Egypt, when the Roman general intervened in a civil war between Cleopatra and her younger brother Ptolemy XIII, supporting Cleopatra's claim to the throne. An Egyptian demotic stela recovered from the Serapeum at Memphis, the great temple complex of the god Serapis, records his birth date with precision, and the infant was given the full royal name Ptolemy XV Caesar, though the world would know him by his nickname, Caesarion, the Little Caesar. Cleopatra had him recognised as Caesar's son, and Mark Antony later testified before the Roman Senate that Caesar had privately acknowledged the boy to his closest associates, though Caesar never officially named him heir in his will, which instead adopted his grandnephew Octavian as his successor.

In late 46 BCE, when Caesarion was still an infant, Cleopatra travelled to Rome at Julius Caesar's invitation and took up residence in his private villa, the Horti Caesaris, outside the city walls. Caesar placed a gilded statue of Cleopatra in the Temple of Venus Genetrix, the temple he had dedicated to his family's divine ancestress in the Forum Julium, a public declaration of her status that scandalised Roman opinion. The infant Caesarion grew up in the household of the most powerful man in the Mediterranean world, surrounded by the marble and bronze of a city that would one day demand his death. But the idyll ended on 15 March 44 BCE, when Caesar was assassinated by a conspiracy of senators led by Brutus and Cassius on the floor of the Theatre of Pompey. Cleopatra fled Rome with her two-year-old son in mid-April, returning to Alexandria before the political storm could engulf them.

Back in Egypt, Cleopatra moved swiftly to secure her son's position. Her younger brother and nominal co-ruler, Ptolemy XIV, died in suspicious circumstances, probably poisoned on her orders, and on 2 September 44 BCE the three-year-old Caesarion was officially proclaimed King of Egypt. He received the royal epithets Theos Philopator Philometor, the God Who Loves His Father and Mother, and though Cleopatra retained absolute autocratic power, the boy was the figurehead of a dynasty that claimed descent from Alexander the Great. Cleopatra commissioned a birth house at the Temple of Montu in Armant, the war god's sanctuary in Upper Egypt, and its decorative reliefs depicted the divine birth of Caesarion in the manner of the pharaohs of old: the god Amun disguised as Caesar, the queen as the goddess Mut, and the child as the divine son Horus, the falcon-headed sky god whose eyes were the sun and the moon. On Cypriot coinage minted in 44 BCE, the infant Caesarion appears in his mother's arms, a tiny king already bearing the weight of empire.

For the next decade, Caesarion grew up in the shadow of his mother's political genius. Cleopatra allied herself with Mark Antony, one of the three men who had divided the Roman world among themselves after Caesar's death, and together they ruled the eastern Mediterranean as partners in power and love. In 34 BCE, Antony staged the Donations of Alexandria, a theatrical ceremony in which he distributed eastern kingdoms to Cleopatra and her children. Caesarion was proclaimed a god, a son of a god, and "King of Kings," a title unprecedented in the management of Roman client-king relationships and one that directly threatened Octavian, whose entire claim to authority rested on his status as Caesar's adopted son. Antony also declared Caesarion to be Caesar's true son and heir, a proclamation that Octavian used to whip up Roman resentment and justify the war that would follow. The breach between the two triumvirs was now fatal.

The war came in 31 BCE. Octavian's fleet met Antony and Cleopatra's forces at Actium, a promontory on the western coast of Greece, and destroyed them. Antony and Cleopatra fled to Alexandria, and Octavian pursued them across the sea. Cleopatra, realising that the game was lost, made plans for escape. She sent the seventeen-year-old Caesarion to Berenice, a seaport on the Red Sea coast of Upper Egypt, with a great treasure and instructions to flee to India if necessary. The plan was sound: Caesarion was young, he was the son of Caesar, and he could have become the rallying point for resistance to Rome in the East. But Octavian was cunning as well as ruthless. He sent false messages to Berenice promising Caesarion the kingdom of Egypt if he returned, and the boy, trusting or desperate, came back to Alexandria.

Octavian captured Alexandria on 1 August 30 BCE. Eleven days later, on 12 August, Mark Antony and Cleopatra died by suicide, traditionally said to have taken their own lives by asp bite and poison rather than submit to Roman captivity. For a few days, Caesarion was the nominal sole pharaoh of Egypt, though Alexandria had already fallen and he remained in hiding. Then Octavian gave the order. According to Plutarch, the Greek biographer who wrote the lives of Caesar, Antony, and other great men of Rome, Octavian followed the advice of his companion Arius Didymus, a philosopher and scholar, who told him: "Too many Caesars is not good" - a pun on a line in Homer. Caesarion was executed in late August 30 BCE, probably on 29 August, the beginning of the Egyptian new year. He was seventeen years old. Octavian also executed Antyllus, Mark Antony's eldest son by his Roman wife Fulvia, but showed mercy to Antony's younger children with Cleopatra, sending them to be raised by his sister Octavia in Rome. Egypt was annexed as a Roman province, and the office of pharaoh ceased to exist.