One of his most famous film roles was in To Kill a Mockingbird (1962), in which he portrayed Walter Cunningham, a client of the main character, lawyer Atticus Finch.

[5] In New York, he gradually gained stage roles, with Broadway credits including Key Largo (1940), Liberty Jones (1941), Fragile Fox (1954), Bus Stop (1955), Orpheus Descending (1957), and Winesburg, Ohio (1958).

[6] From 1945 until his death in 1966, Denton also starred in many films, including The Great St. Louis Bank Robbery (1959) with Steve McQueen in his first leading film role, The Parent Trap (1961) with Maureen O'Hara and Brian Keith, Birdman of Alcatraz (1962) with Burt Lancaster, To Kill a Mockingbird (1962) with Gregory Peck, and Bus Riley's Back in Town with Ann-Margret and Michael Parks.

Denton made two guest appearances on the CBS courtroom drama series Perry Mason with Raymond Burr.

[8] Denton won an Outer Critics Circle Award for Best Performances in Supporting Roles for 1954-1955 for his work in Bus Stop (1955).