He is best remembered for his work as the first host of the TV game shows Beat the Clock and To Tell the Truth, but he was also famous in the roles of Clark Kent / Superman on radio and in animated cartoons, initially in theatrical short subjects and later on television.

[citation needed] He held starring or major supporting roles in The Man I Married (as Adam Waring);[3] Kate Hopkins, Angel of Mercy (as Tom);[4] Pretty Kitty Kelly (as Michael Conway);[5] Terry and the Pirates (as Pat Ryan); Renfrew of the Mounted (as Renfrew); and Abie's Irish Rose (as Abie Levy).

Collyer supplied the voices of both Superman and his alter ego Clark Kent, opposite radio actress Joan Alexander as Lois Lane.

In 1966, Collyer reprised the role in the Filmation animated television series The New Adventures of Superman, reunited with Alexander as Lois Lane.

Collyer did an excellent job keeping the show fast-paced; he spoke quickly and brightly, and was often moving around the stage as much as the contestants.

One of Collyer's trademarks on the show was securing his long-tubed stage microphone in his armpit (particularly while demonstrating the basics of a stunt for his contestants).

When children were brought onstage with their parents, he would take time to talk to each of them and ask them what they wanted to be when they grew up, in a manner reminiscent of his contemporary, Art Linkletter.

At the height of the show's popularity, an installment of The Honeymooners (which surfaced years later, when Jackie Gleason released the so-called "Lost Episodes") featured blustery Ralph Kramden and scatterbrained Ed Norton appearing on and playing Beat the Clock.

Because the show depended on conversation instead of physical stunts, Collyer's demeanor on To Tell the Truth was much calmer and more avuncular than his fever-pitch performances on Beat the Clock.

After the celebrities voted for their choices, Collyer intoned the famous phrase, "Will the real... John Doe... please... stand up?"

The sequence provided an especially riotous moment in 1962, when Collyer purred, with a particularly pronounced twinkle, "Will the real... Bob Miller... please... stand up?"

Butterfield rose, then joined a small band onstage to play and sing his signature song, "Born in Chicago."

Among the celebrities who served as To Tell The Truth panelists during the 14-year run of the show were Tom Poston, Peggy Cass, Orson Bean, Kitty Carlisle (the foregoing foursome was the resident panel in the weekday series), Don Ameche, Peter Lind Hayes, Johnny Carson, Ralph Bellamy, Polly Bergen, Mimi Benzell, Sally Ann Howes, Hy Gardner, Betty White, Phyllis Newman, and Robert Q. Lewis.

On Beat The Clock, he often delivered public service messages about such charitable causes as the March of Dimes and other drives for research of diseases.

When producers Mark Goodson and Bill Todman planned to revive To Tell the Truth for syndication, they wanted Collyer to once again host the show.

"[6] Collyer died at age 61 from a circulatory ailment in Greenwich, Connecticut, on the same day the new To Tell The Truth premiered in daytime syndication.