The Orchard Keeper is set during the inter-war period in the hamlet of Redbranch, a small, isolated community in Tennessee. Its story revolves around three characters: Uncle Arthur Ownby, an isolated woodman who lives beside a rotting apple orchard, John Wesley Rattner, a young mountain boy, and Marion Sylder, an outlaw and bootlegger. The novel begins with Marion picking up a hitchhiker named Kenneth Rattner. Kenneth attacks Marion with a tire iron, attempting to murder and rob him. After a struggle, Marion strangles Kenneth to death. Marion dumps the corpse in a spray pit on Arthur Ownby’s property, as he knows the land well from his frequent pickups of bootleg whiskey. Arthur soon discovers the corpse, but instead of informing the authorities, he transforms the pit into a kind of shrine or crypt to protect and honor the body. As time passes, Kenneth’s wife, Mildred, and son, John Wesley, come to accept he has likely been killed, and John Wesley makes a vow to one day take vengeance on his father’s killer. One night, as Marion is picking up a shipment of whiskey hidden on Arthur’s property, he witnesses Arthur unloading a shotgun into a tank the government has installed on his land. Unnerved, Marion collects the whiskey and flees the property, fearing Arthur might do him harm. Arthur passively watches Marion's car drive off into the night. Marion’s car careens off the road and into a stream. John Wesley happens to be checking some animal traps in the area and, hearing the crash, comes to Marion’s aid, helping the injured man to land. John Wesley is oblivious that Marion is his father’s killer, and Marion does not recognize John Henry as his father’s son. Grateful for his help, Marion gives John Henry one of his dogs, and the two men develop a friendly, almost father and son relationship, with Marion teaching John Henry how to hunt. The local police discover Marion’s vehicle in the stream, its whiskey cargo still intact, as well the defaced government tank. John Wesley becomes a suspect, and is threatened with criminal charges if he doesn’t admit that Marion was driving the whiskey-filled car. John Wesley refuses to cooperate. The police then go to Arthur’s cabin to question him. As they pull up in his yard, Arthur comes out of the cabin wielding a shotgun. The officers call for backup, and a shootout ensues. Arthur wounds several of the officers, then flees, but is captured a short while later. Sylder, too, is captured, when his new vehicle breaks down a bridge, its trunk filled with whiskey. Arthur is diagnosed as insane or senile, and is sent to a mental hospital, where he will likely live out the remainder of his days. Sylder gets sentenced to three years in prison for illegally transporting whiskey. Still oblivious to Sylder’s role in his father’s death, John Wesley leaves Redbranch. He returns several years later to find the town abandoned.
Like much of McCarthy's work, the Orchard Keeper's central themes are highly Biblical in nature: innocence, the end of days, and the relationship between fathers and sons. Both Arthur and Marion take on mentor relationships with John Wesley, acting as surrogate fathers. Ironically, Marion killed John's father, and Arthur tends to the corpse, which, unbeknownst to John, is concealed in Arthur's spray pit. The dense woodlands of Red Branch, described by McCarthy in gorgeous and elaborate detail, are a kind of Eden, in which characters live in a state of ignorant bliss. This bliss is slowly eroded over the course of the novel, as violence, death, decay, and modern civilization slowly but inevitably encroach on Arthur's, John's, and Marion's way of life. The novel ends with John Wesley returning to Red Branch after spending several years out West, only to find the hamlet abandoned and dilapidated. Like Adam and Eden, John Wesley can never return to his idyllic place of birth; it has been forever lost to him.
Kenneth Ratner is an unemployed hitchhiker who attempts to rob and kill Marion Sylder. Sylder strangles him to death, and dumps his corpse in Arthur's spray pit.
John Wesley Rattner is the son of Kenneth Rattner. Throughout most of the novel, he is around the age of 14. No physical description of him is ever given, but McCarthy alludes that he lives alone with his mother. John Wesley is loyal, highly independent, and good natured.
Marion Sylder is an outlaw, bootlegger, and murderer. Sylder is married, but his relationship with his wife is never expanded upon.
Arthur Ownby, also referred to as "The Old Man" and "Uncle Ather", is a hermit who lives alone with his dog in the wilderness. He is acquainted with some of the local boys, eventually including John Wesley.