The film opens with a quote from the Book of Job.
Afterwards, a mysterious, wavering light that resembles a flame flickers in the darkness. Mrs. O'Brien (Jessica Chastain) recalls a lesson taught to her that people must choose to either follow the path of grace or the path of nature. In the early 1970s, she receives a telegram informing her of the death of her son, R.L., at age nineteen. Mr. O'Brien (Brad Pitt) is notified by telephone while at an airport. The family is thrown into turmoil.
In the 2000s, eldest son Jack O'Brien (Sean Penn) is adrift in his modern life as an architect. One day he has an argument with his father regarding R.L.'s death. Later, after Jack sees a tree being planted in front of a building, he begins to reminisce about his life as a young teenager during the 1960s.
The universe is formed, including the Milky Way galaxy and the Solar System. Voices ask various existential questions. On the newly formed Earth, volcanoes erupt and microbes begin to form. Early sea life is shown, then plants on land, then dinosaurs. From the vantage point of space, an asteroid is seen impacting the Earth. (For these sequences, the music is "Lacrimosa," a movement from Zbigniew Preisner's Requiem for My Friend .)