Angel's Egg follows the daily life of an unnamed young girl in a surreal world of darkness and shadows.
The girl is the keeper of a mysterious egg. She spends her time collecting bottles and artifacts in a gothic, abandoned city. An unnamed man arrives in the dark town one day riding a machine, wearing a cross-like weapon on his back and having bandaged hands. The two meet and talk, though their dialogue consists mostly of the single, repeated question "Who are you?"
Meanwhile, the shadows of giant coelacanths appear within the town, and then the many human statues which line it come to life and begin hunting the fishes with spears. This scares the girl and the man holds her protectively under his long coat. The girl leads the man out the city toward a strange rock where she lives and they come across a carving of a strange tree. The man tells the girl that he has seen it before but is unable to remember where.
Inside the girl's vast cavernous "refuge", which contains many strange fossils and her collection, the man tells the girl the story of Noah's Ark, but changes the climax of that story. He waits for the girl to fall asleep and breaks the egg.
The girl reacts in anguish and follows the departing man, only to fall into a ravine of water and die. Her dying exhalation under the water blossoms into bubbles of "eggs" on the surface. The film ends with the man standing alone on a desolate beach as a strange machine rises from the ocean carrying a statue of the girl and ascends for the heavens as the "world" being revealed as a settlement on the edge of a hollow shell floating through an endless sea, though this is not elaborated upon.