On October 2, 1988, in the small town of Middlesex, Virginia, intellectual but troubled teenager Donald J. "Donnie" Darko has been experiencing bouts of sleepwalking and wakes up on a road before cycling home. Later that night, led by a mysterious voice, he sleepwalks out of his home. Once outside, he meets a figure in a monstrous rabbit costume who Donnie comes to refer to as Frank and tells Donnie that the world will end in 28 days, 6 hours, 42 minutes and 12 seconds. Donnie wakes up the next morning on a local golf course and returns home to discover a jet engine has crashed into his bedroom. His older sister Elizabeth tells him the FAA investigators do not know its origin.
Over the next several days, Donnie continues to have visions of Frank. His parents, Eddie and Rose, consult with his psychiatrist, Dr. Thurman. She believes he is detached from reality and that his visions of Frank are "daylight hallucinations" due to paranoid schizophrenia. Frank begins to influence Donnie's actions through his sleepwalking episodes, including causing him to flood his high school by breaking a water main. Donnie also starts seeing Gretchen Ross, who has recently moved into town with her mother under a new identity to escape her violent stepfather. Dr. Thurman hypnotizes Donnie at his next therapy session, but it ends with him discussing his sexual fantasies involving Christina Applegate while he unzips his pants, causing Thurman to end the session prematurely. Later, Donnie goes to a clearing and shoots bottles while his friends discuss the sexual components of Smurfs. While there, Donnie has an encounter with a seemingly senile old woman, nicknamed Grandma Death by the locals, who whispers in his ear "every creature on Earth dies alone". Donnie later brings this up in one of his therapy sessions, admitting he doesn't want to be alone.
Gym teacher and Christian fundamentalist Kitty Farmer attributes the act of vandalism to the influence of the short story The Destructors, assigned by dedicated English teacher Karen Pomeroy. Kitty begins teaching "attitude lessons" taken from local motivational speaker Jim Cunningham, but Donnie rebels against these, leading to friction between Kitty and Rose who both have young daughters in the same dance troupe. While on a date with Gretchen at the local cinema, Donnie envisions Frank with one of his eyes shot out. Frank asks Donnie, who in turn asks his science teacher, Dr. Kenneth Monnitoff, if he believes in time travel. Monnitoff gives Donnie some information on the topic, but later cuts their sessions short out of fear of losing his job, but not before giving Donnie The Philosophy of Time Travel, a book written by a former nun called Roberta Sparrow who has since become Grandma Death. Later, while watching football, Donnie notices bubbly columns emerging from the chests of people around him that show Donnie where the person will move, matching illustrations from Sparrow's book. A bubble appears on his chest and he follows it to his parents' closet where he finds and takes a gun.
Kitty arranges for Cunningham to speak at a school assembly, where Donnie insults him while offering his own advice to other children who had voiced their fears to Cunningham. He later finds Cunningham's wallet and address, and Frank suggests setting his house on fire, which Donnie does. Firefighters discover a hoard of child pornography there. Cunningham is arrested, and Kitty, who wishes to testify in his defense, asks Rose to take her place as chaperone for their daughters' dance troupe on its trip to Los Angeles.
With Rose and their little sister Samantha in Los Angeles, and Eddie away for business, Donnie and Elizabeth hold a Halloween costume party to celebrate Elizabeth's acceptance to Harvard. At the party, Gretchen arrives distraught as her mother has gone missing which she assumes was caused by her stepfather, and it is implied that she and Donnie have sex for the first time. When Donnie realizes that Frank's prophesied end of the world is only hours away, he takes Gretchen and two other friends to find Sparrow. Instead, they find two high school bullies, Seth and Ricky, trying to rob Sparrow's home. Donnie, Seth, and Ricky fight in the road in front of her house, just as she returns home. Donnie's two friends and the bullies flee when an oncoming car runs over Gretchen, killing her. The driver is Elizabeth's boyfriend, Frank Anderson, wearing the same rabbit costume from Donnie's visions. Donnie shoots him in the eye with his father's stolen gun, and walks home carrying Gretchen's body.
Donnie returns home as a vortex forms over his house. He takes one of his parents' cars, loads Gretchen's body into it, and drives to a nearby ridge that overlooks town. There, he watches as the plane carrying Rose and the dance troupe home from Los Angeles gets caught in the vortex's wake, which rips off and catches one of its engines. Events of the previous 28 days rewind. Donnie wakes up in his bedroom, recognizes the date is October 2, and laughs as the jet engine falls into his bedroom, crushing him. Around town, those whose lives Donnie would have touched wake up from troubled dreams. Gretchen, who in this timeline had never met Donnie, bikes by the Darko home the next morning and learns of his death. She and Rose exchange glances and wave as if they know each other but cannot remember from where.
Jake Gyllenhaal as Donnie Darko
Holmes Osborne as Eddie Darko
Maggie Gyllenhaal as Elizabeth Darko
Daveigh Chase as Samantha Darko
Mary McDonnell as Rose Darko
James Duval as Frank Anderson
Arthur Taxier as Dr. Fisher
Patrick Swayze as Jim Cunningham
David St. James as Bob Garland
Jazzie Mahannah as Joanie James
Jolene Purdy as Cherita Chen
Stuart Stone as Ronald Fisher
Gary Lundy as Sean Smith
Alex Greenwald as Seth Devlin
Beth Grant as Kitty Farmer
Jena Malone as Gretchen Ross
Seth Rogen as Ricky Danforth
David Moreland as Principal Cole
Noah Wyle as Prof. Kenneth Monnitoff
Drew Barrymore as Karen Pomeroy
Kristina Malota as Susie Bates
Marina Malota as Emily Bates
Carly Naples as Suzy Bailey
Tiler Peck as Beth Farmer
Patience Cleveland as Roberta Sparrow ("Grandma Death")
Katharine Ross as Dr. Lillian Thurman
Lisa K. Wyatt as Linda Connie
Rachel Winfree as Shanda Riesman
Jack Salvatore Jr. as Larry Riesman
Lee Weaver as Leory
Phyllis Lyons as Anne Fisher
Ashley Tisdale as Kim
Jerry Trainor as Lanky Kid