John Dehner began his career as an animation assistant at Walt Disney Studios, worked as an Army publicist during WWII and, as a Los Angeles radio news reporter, editor and announcer, netted his station a Peabody Award for his coverage of the first UN conference in San Francisco in the late 1940s. Dehner started acting in films in the mid-1940s, eventually appearing in over 100 features, mostly westerns or action films. As sheriff Pat Garrett, he proved a notable foil to Paul Newman's Billy the Kid in Arthur Penn's "The Left-Handed Gun" (1958).

Once voted "best radio voice" by "Radio Life Magazine," Dehner was a prolific radio performer during the 1950s, starring as J.B. Kendall, a Brit in the American West, on "Frontier Gentleman" and as Paladin on "Have Gun Will Travel." Throughout the 60s and 70s he made regular appearances on TV series including "The Westerner" (1960), "The Roaring Twenties" (1960-62), "The Don Knotts Show" (1970-71) "The Doris Day Show" (1971-73) and "Big Hawaii" (1977). Later roles included Secretary of State Dean Acheson in the miniseries "The Missiles of October" (1974); Admiral Ernest King in the miniseries "The Winds of War" (1983); Henry Luce in "The Right Stuff" (1983); and the judge in "Jagged Edge" (1985).