Intruder in the Dust is a novel about racial injustice and the larger role of race relations in a small town in Mississippi in the 1940s. William Faulkner demonstrates that the threat of violence against black people is a constant reality that affects all of their actions. A few people in the novel, both black and white, step up and take responsibility for helping achieve justice in the town. Ultimately, they do have an impact, and justice is served.

A young white boy, Chick Mallison, and an elderly African American man, Lucas Beauchamp, find their lives linked when the older man treats the boy kindly, literally saving his life. The bonds of obligation provide an ongoing connection between the two that Chick, though a teenager, takes very seriously.

Chick, while out hunting in the winter, falls through thin ice. Lucas happens to see the accident and rescues him, then takes him home to dry out and get warm. Because they live in a small town, Chick knows that Lucas is a proud man and is even defiant towards white people. After being saved by Lucas, Chick makes numerous efforts throughout the following years to repay what he understands as his debt to Lucas. He cannot figure out how to do this effectively, and each effort is countered by Lucas, who also detests the idea of moral and financial debt.

The novel's conflict and resolution revolves around a murder—which turns out to be a fratricide between two members of a poor white family, many of whom live out in the woods away from town. This truth is not revealed until much later in the novel, however. Instead, the reader learns that a man named Vinson Guthrie has been murdered, and Lucas has been accused of this crime.

Chick understands that mob violence will probably take the place of court justice if nothing is done, so he decides to help defend Lucas, both in his murder trial and from the violent people of the town. Chick's uncle is a lawyer and, after considerable urging on Chick's part, agrees to defend Lucas. Chick's friend Aleck, who is black, and the elderly Miss Habersham, who had grown up with Lucas's wife (now deceased), are also involved in the efforts to help Lucas.

The boys (through serious deliberation) decide that the corpse of the victim will provide valuable evidence of Lucas's innocence, so they dig it up—only to find a different man's body in the grave. This information is enough to convince the sheriff to look into the case again.

The dead man who they unearthed was actually Jake Montgomery, with whom Crawford Guthrie, the deceased's brother, had some business connections. Crawford is ultimately exposed as the killer of both men, motivated by the attempt to cover up his illegal activities. Lucas is freed, and Crawford is brought to justice—but he takes his own life while in prison.

Chick then believes that he and Lucas are even, but the older man insists on paying a fee for the services, requiring a receipt for the two dollars.