Before the events of the film, Joe had tried to farm for a living, but was unable to make ends meet, and the bank eventually foreclosed on his property. He became a police officer as a way to support his young wife and child, and is a conscientious, upstanding, productive member of society. However, Joe has his own demons to fight with. The opening shot of the film shows a car chase which ends with Joe using his gun to kill a man in self-defense. This results in Joe's conflicted feelings about killing the criminal, as well as the praise and scorn from members of his community from this shooting. Frank, who had been involved with run-ins with the law before going to Vietnam, is described by his father as having "restlessness." Upon his return to town, he breaks into his brother's home and is nearly shot by Joe's wife. The next day, Frank leaves town without ever stopping by his parents' home. As Joe states in the narration, Frank was correct in his assessment that his parents would understand, as they seem to have an understanding of Frank's ways.
Joe does not hear from his brother for some time, but eventually discovers that he is in jail in another state from their father, who had kept the information quiet to avoid upsetting the brothers' mother. In jail, Frank demonstrates his outgoing personality, along with his continued tendency toward violence. Upon release, Frank returns to his hometown, settles down and finds a job, but is unable to reconcile his wandering, angry violent nature with this lifestyle.
The film explores the inner and outer conflicts the two brothers face as adulthood and the resulting responsibilities come to bear upon them.
Critic Roger Ebert has noted how the two brothers in this film represent not only the two sides of manhood in society, but also, possibly, the two sides of Sean Penn's own character.
Penn and Phillips sent Mortensen the script while he was making Young Guns II in Tucson, Arizona and flew there to meet with him. The actor agreed to star in Penn's film. Penn had David Morse and Mortensen rehearse their pivotal scene in a bar for two weeks. The director had a bar set up in a gymnasium which allowed the actors to blow off steam by shooting baskets in between rehearsals. While making the film, Penn felt that Mortensen's "inherent kindness" was too visible and had him work with a member of the Hell's Angels motorcycle club that the director knew in order to acquire an edginess that Penn felt necessary for the character.
The Indian Runner is the last film to feature Sandy Dennis before her untimely death.