Carradine appeared in ten John Ford productions, including The Grapes of Wrath (1940), portrayed the Biblical hero Aaron in The Ten Commandments (1956), and also did considerable stage work, much of which provided his only opportunity to work in a classic drama context, and appeared on Broadway. He appeared in more than 200 movies sometimes playing eccentric, mad or diabolical characters, especially in the horror genre with which he had become identified as a "star" by the mid-1940s. He also made numerous television cameos (notably on The Munsters, in recurring guest appearances as mortician Mr. Gateman).

For his contribution to the motion picture industry, John Carradine has a star on the Hollywood Walk of Fame at 6240 Hollywood Blvd. In 2003, he was inducted into the Western Performers Hall of Fame at the National Cowboy & Western Heritage Museum in Oklahoma City, Oklahoma.

Carradine's idiosyncratic habit of strolling Hollywood streets while reciting Shakespearean soliloquies earned him the nickname "Bard of the Boardwalk".