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, who 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 peach 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 vows 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 thegovernment 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 unaware that Marion is his father’s killer, and Marion does not recognize John Wesley as the son of the man he killed. Grateful for his help, Marion gives John Wesley one of his dogs, and the two men develop a friendly, almost father and son relationship, with Marion teaching John Wesley 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 on 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 rolein his father’s death, John Wesley leaves Redbranch. He returns several years later to find the town abandoned.