Hypnos was born in the primordial darkness, the son of Nyx, the goddess of Night, one of the oldest beings in the Greek cosmos, born from Chaos itself. The poet Hesiod, writing in the eighth or seventh century BCE, tells us in his Theogony that Nyx bore Hypnos and his twin brother Thanatos without a father, as she had borne Doom and Death and the tribe of Dreams before them. In some accounts, particularly those of the Roman mythographer Hyginus and the philosopher Cicero, his father is named as Erebus, the personification of darkness itself. The brothers were inseparable from birth: Thanatos, the pitiless god of peaceful death, with a heart of iron, and Hypnos, the gentle god of sleep, who eased the suffering of mortals and gods alike. They dwelled together in the underworld, in a cave so deep that the sun's rays never touched it, near the river Lethe, the waters of forgetfulness that flowed from the realm of the dead.

The cave of Hypnos was a place of perfect silence. The Roman poet Ovid, in the eleventh book of his Metamorphoses, describes it in vivid detail: the entrance was hidden by countless white and red poppies, the flowers from which the juice of sleep is extracted, and the river Lethe murmured softly at the cave's mouth with a sound so monotonous that it invited slumber rather than waking. Inside, the god lay upon a couch of black ebony with a bed of down and a coverlet the colour of night. Around him swirled his innumerable sons, the Oneiroi, the spirits of dreams, more numerous than the grains of sand on the seashore. Chief among them were Morpheus, who shaped dreams in the forms of men; Icelus, also called Phobetor, who brought dreams of beasts and monsters; and Phantasos, who created dreams of lifeless things. The dreams passed each night through one of two gates: the gate of horn, through which passed true and prophetic dreams, and the gate of ivory, through which passed false and deceptive ones.

Hypnos's most famous appearance in myth comes in the fourteenth book of Homer's Iliad, the epic of the Trojan War. Hera, the queen of the gods and wife of Zeus, wished to aid the Greeks, whom Zeus had forbidden the gods to help. She needed her husband asleep and unaware. She went to Hypnos on the island of Lemnos, where he dwelled, and begged him to put Zeus to sleep. At first Hypnos refused. He reminded Hera of a previous occasion when he had done her this favour: he had lulled Zeus to sleep so that Hera could send a storm to torment Heracles, the hero who had sacked Troy, as he sailed home. When Zeus awoke and discovered the deception, he had hunted Hypnos through the halls of Olympus in a rage, and only the intervention of Nyx, Hypnos's mother, whose power even Zeus feared, had saved him from being cast into the sea. But Hera was determined. She offered Hypnos a golden throne, imperishable forever, crafted by Hephaestus, the divine smith. When he still hesitated, she offered him what he truly desired: the hand of Pasithea, one of the three Graces, the goddesses of charm and beauty, in marriage. Hypnos could not resist. He agreed, and when Hera had seduced Zeus on Mount Ida in the Troad, Hypnos, in the form of a bird, perched in the branches of a pine tree above them and poured sleep upon the king of the gods. Then he flew to Poseidon, the god of the sea, to tell him that Zeus slept, and Poseidon rallied the Greeks to turn the tide of battle.

In the sixteenth book of the Iliad, Hypnos appears again in a gentler role. Sarpedon, the son of Zeus and a mortal woman, had been killed by Patroclus, the beloved companion of Achilles, the greatest Greek warrior. Zeus, grieving for his son, wished to rescue the body from the battlefield, and he commanded Apollo, the god of light and prophecy, to do so. Apollo cleansed the body of blood and dust and handed it to Hypnos and Thanatos, the twin brothers, who carried it swiftly across the sea to the rich countryside of Lycia, where Sarpedon's family gave him burial with tomb and gravestone. It was a scene of perfect tenderness: the god of sleep and the god of death, winged and gentle, bearing the hero home in their arms, their inverted torches extinguished, their faces calm.

Hypnos appears in other myths as well. When Selene, the goddess of the moon, fell in love with Endymion, the beautiful shepherd, and could not bear to watch him age and die, she appealed to Hypnos. He granted the mortal eternal sleep, and in some accounts he let Endymion sleep with his eyes open so that he could gaze upon Selene forever. In the story of Jason and the Argonauts, Medea, the sorceress daughter of King Aeetes of Colchis, called upon Hypnos to put to sleep the dragon that guarded the Golden Fleece, allowing Jason to steal it. Hypnos was married to Pasithea, as Hera had promised, and their union produced the endless tribe of dreams that still visit the sleeping world each night. In art he was depicted as a beautiful winged youth, sometimes with wings on his shoulders, sometimes on his temples, holding poppies or an inverted torch or a horn dripping with the waters of Lethe. The Greeks did not worship him with temples or sacrifices, but they knew his power every time they closed their eyes.