In October 1988, in Middlesex, Virginia; Donnie Darko (Jake Gyllenhaal), a troubled teenager, appears to be suffering the symptoms of paranoid schizophrenia. At the start of the film, he has recently stopped taking his medication. His parents, Rose and Eddie (Mary McDonnell and Holmes Osborne) and his sisters, Elizabeth and Samantha (Maggie Gyllenhaal and Daveigh Chase), are concerned about him. One night at dinner, Donnie and his sister get into a profane argument during which Elizabeth reveals she knows Donnie is no longer taking his medication. Rose confronts Donnie in his bedroom asking him where her little boy has gone and who is the stranger that has taken his place. As she leaves the room, she hears him call her a "bitch" from the other side of the door. Feeling guilty, Donnie resumes taking his medication. On October 2, however, he sleepwalks and meets Frank (James Duval), a man in a menacing bunny costume. Frank tells him that in 28 days, 6 hours, 42 minutes and 12 seconds, the world will end. While he is outside, a jet engine mysteriously crashes through the roof of the Darkos' house, destroying Donnie's bedroom.
As Eddie drives Donnie to the office of Dr. Thurman (Katharine Ross), Donnie's therapist, Eddie nearly runs over Roberta Sparrow, also known as "Grandma Death" (Patience Cleveland). A senile old woman who spends her days walking back and forth from her house to the mailbox across the street, Grandma Death whispers in Donnie's ear that "every living creature on this earth dies alone". This greatly troubles Donnie, who worries that life has no meaning.
A few days later, Frank appears to Donnie in a hallucination and urges him to flood the school that he attends by breaking open the water main with an axe. Donnie also embeds the axe in the head of the school's solid bronze statue of its mascot and spray-paints "They made me do it" on the sidewalk. School is canceled that day and Donnie walks the new girl, Gretchen Ross (Jena Malone), home. She reveals that her stepfather nearly killed her mother and hasn't been caught. Donnie reveals his own troubled past as well as his intelligence. Gretchen calls Donnie weird (which was a compliment in her case), prompting Donnie to nervously ask Gretchen to date him, which she agrees to.
Frank continues to appear to Donnie and tells Donnie that he can do anything and won't get caught. Frank also tells Donnie about time travel, further confusing him. Soon, Donnie sees tubes of fluid light extending out of his family's chests, indicating where they will go. His own tube beckons him to follow as it enters his parents' room and reveals the gun his father keeps in a box in the closet. Donnie speaks about time travel with Dr. Monnitoff who gives him a book, The Philosophy of Time Travel, written by Roberta Sparrow. She used to be a nun and a teacher at the high school. However, the climate at the school is becoming increasingly polarized as Kitty Farmer leads a protest against Ms. Pomeroy's choice of reading material; one of the stories she had assigned, Graham Greene's "The Destructors," features teenagers who flood a man's house by breaking a water pipe. Ms. Pomeroy is fired and Dr. Monnittoff, who is also her boyfriend, refuses to discuss time travel with Donnie once his questions take a theological direction for fear he could also lose his job.
Gretchen and Donnie grow closer. She is one of the few people he opens up to about his time travel visions, and they discuss how they wish they could travel back in time and prevent the bad things in their lives from happening. Dr. Thurman increases Donnie's medication and begins hypnotherapy with him. But Frank continues to appear to Donnie. One night, Donnie and Gretchen go to see the cult horror film The Evil Dead. Gretchen falls asleep and Frank appears. When Donnie asks Frank why he wears a "stupid bunny suit," Frank asks Donnie why he wears a "stupid man suit," then acquiesces and takes the head off, revealing a young adult (who looks like Elizabeth's boyfriend, Frank) with a gruesome wound in his right eye. When Donnie asks about the cause of the eye wound, Frank replies "I am so sorry". Frank asks if Donnie has "ever seen a portal?" and then directs Donnie's attention to the movie screen. A portal opens, revealing the house of Jim Cunningham (Patrick Swayze), a ludicrous (but highly followed) motivational speaker. Frank tells Donnie to burn it to the ground. Donnie leaves the sleeping Gretchen in the theatre and does as Frank tells him to. He is not caught, and firefighters discover a dungeon of child pornography in a hidden room in the mansion. Cunningham is arrested the next morning. Kitty Farmer, a friend and devoted follower of Cunningham's, is convinced he has been framed and decides she must lead his public defense. She asks Rose to take her place accompanying the school's dance team, Sparkle Motion, to Los Angeles to appear on Star Search. Samantha is Sparkle Motion's lead dancer and, against her better judgment, Rose agrees. Eddie is away on business, so this means Elizabeth and Donnie are on their own.
Elizabeth is accepted into Harvard, and she and Donnie decide to throw a Halloween party to celebrate. The night of the party (October 30), Gretchen comes to Donnie's house for safety because her mother has suddenly disappeared. Donnie comforts her and repeatedly ignores phone calls from his desperate therapist (who knows that Donnie is responsible for the vandalism to the high school and Jim Cunningham's house) and Rose, who calls to announce that Sparkle Motion won their initial Star Search competition and that they will return on a red eye flight that night.
At midnight, Donnie has another hallucination about the fluid light tunnels. He realizes that the 28 days have passed, and that only 6 hours remain until the end of the world. Convinced that Grandma Death is in some way connected to Frank, Donnie persuades Gretchen and two other friends to leave the party and go with him to her house. When they get there, they are assaulted by the high school's resident bullies (Alex Greenwald and Seth Rogen). In the fight, Gretchen is thrown dazed beside the road. While trying to avoid running over Grandma Death, the car driven by Frank, Elizabeth's boyfriend who is on his way to their Halloween party, is forced out of the road and strikes and kills Gretchen. Frank and his friend get out of the car. Donnie realizes that Frank is wearing the creepy bunny Halloween costume that his hallucination wears. Dismayed, he uses his father's gun to shoot Frank in the right eye, killing him and giving him the exact appearance of his hallucination of Frank in the cinema. He then carries Gretchen's body to his home, steals the car keys from a sleeping Elizabeth and, taking Gretchen's body with him, drives into the hills above town.
From that vantage point, Donnie can see a time tunnel forming over the town. The red eye flight carrying Rose, Samantha and the rest of Sparkle Motion enters the turbulence created by the time tunnel, and one of the engines on the jet breaks free and falls into the tunnel. Donnie looks at Gretchen with love and the primary universe is reset to October 2.
It is once again October 2. Donnie is in bed, creating a predestination paradox. On this occasion however, he chooses to stay in bed, presumably to prevent the harm he caused to several lives in the tangent universe, including Gretchen, the girlfriend he will never meet. Shortly after he goes to sleep, the jet engine from the red eye flight on October 30 crashes through the roof, killing him. All the people affected by Donnie's actions awake as if from a nightmare, having some fragments of memories remaining: Frank, Elizabeth's boyfriend, subconsciously touches his right eye. Jim Cunningham, perhaps in guilt and remorse for being a pedophile, a hypocrite and phony, awakens crying. As Donnie's body is taken away, Gretchen, having never met Donnie, rides by the Darkos' house on her bicycle. She learns from a neighborhood boy what has happened and waves to Rose, who is smoking a cigarette. There is an air of mutual recognition between them.
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