New York-born, Collyer originally sought a career in the law and worked his way through Fordham University by radio acting. Though he became a law clerk after his graduation, making as much in a month of radio as he did in a year of clerking convinced him to make broadcasting his career, changing his surname and becoming a familiar voice on all three major radio networks by 1940. Among others, his radio roles as Terry and the Pirates (Pat Ryan), Renfrew of the Mounted (the title role), and Abie's Irish Rose (the title role, again), not to mention announcing for a number of radio soap operas. But his best-remembered radio role arrived in early 1940: the title role in The Adventures of Superman on the Mutual network, a role he did in the 1940s radio drama and subsequent Superman cartoons.

Collyer got his first helping of game shows when he co-hosted ABC's (the former NBC Blue network) Break the Bank with future Miss America Pageant mainstay Bert Parks; and, when he was picked to host the radio original of the Mark Goodson-Bill Todman team's first game, Winner Take All--the latter also becoming, in due course, the first hosting seat for another game show titan, Bill Cullen.

Collyer went on to host the television versions of both shows, but in 1950 that he got the slot which genuinely made his name: Beat the Clock, a stunt game show which pit couples (usually, but not exclusively, married) against the clock in a race to perform silly (sometimes messy) tasks called "stunts", the grand prizes for which usually came in terms of cash or home appliances. For eleven years (1950-61), Collyer presided over the slapstick, sometimes getting clobbered himself by as much whipped cream as his 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). He was also typically wore bow ties, and liked to point out when contestants were 'bow tie guys' like himself. He enjoyed meeting families of contestants, and was fond of children. He would always ask about contestants' children, and sometimes would compare the number and sexes with that of his own family. 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.

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. Unlike the show's familiar parody of The $64,000 Question (The $99,000 Answer), Gleason's Beat the Clock episode used the actual show, including Collyer and his famous sign-off: "Next week may be your turn to beat the clock."

But Collyer in 1956 became equally if not more familiar as the host of a new Goodson-Todman production, To Tell The Truth on CBS. This panel show featured four celebrities peppering questions at three mystery guests claiming to be the same person, in a bid to determine just which of the three was the person in question, until Collyer purred the famous phrase, "Will the real Such-and-So---please...stand up," always with the pauses---and the actual person would do precisely that. 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?" Two Bob Millers, both pitchers for the newborn New York Mets, rose.

Among the celebrities who served as To Tell The Truth panelists during the fourteen-year run of the show were Orson Bean, Ralph Bellamy, Polly Bergen, Kitty Carlisle, Peggy Cass, Bert Convy, Hy Gardner, Phyllis Newman, and Tom Poston.

There was a side of Collyer's career that tied controversy. During his 1950s heyday with Beat the Clock and To Tell the Truth, he was a leader in an overtly anti-Communist faction of the New York chapter of the American Federation of Radio and Television Artists. That faction supported such publications as Red Channels (the famous list of 151 reputed Communists or reputed fellow travelers, as the term was then, in radio and television) and interest groups that shared the authors' politics---groups like Aware, Inc. (co-founded, in fact, by the man who wrote Red Channels's introduction), purporting to screen broadcast performers for actual or alleged Communist ties, pressuring networks and advertisers to shun them under threat of boycott.

An opposing faction, led by CBS radio personality John Henry Faulk and (ironically enough) To Tell The Truth panelist Orson Bean, defeated Collyer's faction in an election to run the New York local. (This was the election Faulk claimed provoked Aware to name his slate and pressure him off the air---not because he was himself a Communist but because he had once entertained at gatherings deemed pro-Communist---which in turn provoked his famous libel suit, winning in 1963.) Whatever Collyer thought of Bean's actual or alleged politics, or Bean Collyer's, they were nothing but professional and courteous to each other on air. Such was Collyer's professional way with any colleague or guest, no matter what he or they thought or did off the air.

Collyer's other game hosting slots included the short-lived (two years) game, Feather Your Nest, and the ABC game Number, Please in 1961 (which replaced Beat the Clock on the Monday after the final ABC episode).

In 1969, Beat the Clock was brought back for a new syndicated run. The host chosen for the show was Jack Narz. A story goes that Narz was flying to New York to do the first tapings of the show and who should sit next to him on the plane by Bud Collyer. Narz was nervous and didn't know what to expect but was pleased to find Collyer as generous and kind as he appeared on TV. Collyer wished him luck and that his run would be as long as the original, and before the week was done, handwritten notes for every member of the crew who had worked on the original series arrived from Collyer wishing them luck.

Religion was very important to Collyer, and he was always particularly pleased to hear contestants say that they considered donating portions of their winnings to the church. He would often include "God bless you" in his parting words to contestants. He was always extra happy to have a contestant that was a minister on the show and would ask about his congregation. He taught a Sunday school class at his Presbyterian church for more than 35 years, and spent some of his off-time as a caretaker at his church. Collyer was known to have contributed to various Christian religious works, including authoring at least one religious book and making a recording of the Today's English Version New Testament. He was also fond of charitable endeavours and was pleased to hear contestants planning to donate to charities. On Beat the Clock, Bud would often take time to deliver public service messages about such charitable causes as the March of Dimes and other drives for research of diseases.

Collyer died at the relatively early age of 61 from a circulatory ailment in Greenwich, Connecticut in September 1969 - on the same day To Tell The Truth was revived in syndication, hosted by his old friend Garry Moore, and not long after he run-in with Narz.