On the night of May 24, 1856, John Brown and his company of Free State volunteers murdered five men settled along the Pottawatomie Creek in southeastern Kansas. The victims were prominently associated with the pro-slavery Law and Order Party, but were not themselves slave owners. This assault occurred three days after Border Ruffians from Missouri burned and pillaged the anti-slavery haven of Lawrence, and two days after Massachusetts Senator Charles Sumner was severely beaten by Senator Preston Brooks of South Carolina. The action on the 24th occurred at three different houses:

At the Doyle farm, James and two of his sons, William and Drury, were dragged outside and hacked up with short, heavy sabres donated to Brown in Akron, Ohio. Mrs. Doyle, a daughter, and fourteen year old John were spared. The gang then moved on to Allen Wilkinson's place. He was 'taken prisoner' amid the cries of a sick wife and two children. Two saddles and a rifle were apparently confiscated. The third house visited that night was owned by James Harris. In addition to his wife and young child, Harris had three other men sleeping there. Only one of them, William Sherman, was executed. Weapons, a saddle, and a horse were confiscated from the house. While members of the rifle company, including four of Brown's sons, asserted that their Captain did not commit any of the actual murders himself, he was the undisputed leader and made the decisions as to who should be spared.

The combination of the fall of Lawrence and the Pottawatomie killings caused southeastern Kansas to erupt into guerilla warfare. Raiders from Missouri terrorized the Free Soilers, while roving gangs of Free State volunteers inflicted similar violence upon their pro-slavery neighbors. While neither John Brown nor any members of his company were apprehended for their involvement at Pottawatomie, his two eldest sons-- who were with their own rifle company near Lawrence at the time of the murders-- were seized by mobs and nearly lynched. Jason Brown was released relatively quickly, but John Jr. was imprisoned until September. The recent events had also triggered a temporary insanity, from which he did not recover until after his release.

Most of the books written by members of the abolitionist community in the years after Brown's own execution in 1859 downplayed this stain on the otherwise rich career of their holy warrior. James Redpath, the first in a long line of biographers who 'martyred' Brown, denounced the whole episode as a pro-slavery conspiracy to villify both the Hero and the Free Soil cause. The Reverend H.D. Fisher makes mention of the "Pottawatomie Creek disaster", but otherwise extolls the virtues of Brown's selfless crusade for emancipation. An excerpt from Fisher's memoirs, Gun and the Gospel, is not wholly factual but is nevertheless a good example of the type of literature focused on Brown after his death. Brown himself is reputed to have acted evasively whenever asked about the incident, and never admitted his direct responsibility. The Pottawatomie killings remain a gruesome and enigmatic facet of the prelude to War which took place in the Kansas Territory.