The two most noted screen portrayals of Brown have both been given by actor Raymond Massey. The 1940 film Santa Fe Trail, starring Errol Flynn and Olivia de Havilland, depicted Brown completely unsympathetically as an out-and-out villainous madman, and Massey added to that impression by playing him with a constant, wild-eyed stare. The film gave the impression that it did not oppose African-American slavery, even to the point of having a black "mammy" character say, after an especially fierce battle, "Mr. Brown done promised us freedom, but... if this is freedom, I don't want no part of it". Massey portrayed Brown again in the little-known, low-budget Seven Angry Men, in which he was not only unquestionably the main character, but was depicted and acted in a much more restrained, sympathetic way.
Massey along with Tyrone Power and Judith Anderson starred in the acclaimed 1953 dramatic reading of Stephen Vincent Benet's epic poem John Brown's Body Three actors in formal dress recited and acted in a two-hour presentation of the poem. The production toured sixty cities in twenty-eight states. In Book I of his epic poem, Benet called him a stone, "to batter into bits an actual wall and change the actual scheme of things."
Brown was also portrayed on film by John Cromwell in the 1940 Abe Lincoln in Illinois. Cromwell was the director of the film and was not credited in the role. Lincoln was played by Raymond Massey.
Singer Johnny Cash portrayed a noble but unrealistic John Brown in Book I, Episode Five of the 1985 TV miniseries North and South.
Royal Dano portrayed John Brown in the 1971 western comedy Skin Game.
Sterling Hayden also portrayed John Brown in the 1982 miniseries The Blue and the Gray.
In 1938–1940, American painter John Steuart Curry created Tragic Prelude, a mural of John Brown holding a gun and a Bible, in the Kansas State Capitol in Topeka, Kansas. In 1941, Jacob Lawrence illustrated the life of John Brown in The Legend of John Brown, a series of twenty-two gouache paintings. By 1977, the original paintings were in such fragile condition they could not be displayed, and the Detroit Institute of Arts commissioned Lawrence to recreate the series as a portfolio of silkscreen prints. The result was a limited edition portfolio of twenty-two hand-screened prints. The works were printed and published with a poem, John Brown, by Robert Hayden, which was commissioned specifically for the project. Though John Brown had been a popular topic for many painters, The Legend of John Brown was the first to explore the topic from an African American perspective.
The progressive rock band Kansas adapted Curry's painting of John Brown as the cover of their first album, Kansas, released in 1974. A similar image of Brown appears on The Best of Kansas, along with images referencing other previous Kansas albums.
Paintings such as Hovenden's The Last Moments of John Brown immortalize an apocryphal story, in which a Black woman offers the condemned Brown her baby to kiss on his way to the gallows. It was probably a tale invented by journalist James Redpath.