After his first divorce, Belzer relocated to New York City, moved in with singer Shelley Ackerman, and began working as a stand-up comic at Pips, The Improv, and Catch a Rising Star. He participated in the Channel One comedy group that satirized television and became the basis for the cult movie The Groove Tube, in which Belzer played the co-star of the ersatz TV show The Dealers.

Belzer was the audience warm-up comedian for Saturday Night Live and made three guest appearances on the show between 1975 and 1980. He also opened for musician Warren Zevon during his tour supporting the release of his album Excitable Boy.
In the late 1970s and early 1980s, Belzer became an occasional film actor. A short skit of a younger Belzer can be found on Sesame Street in a season 9 episode in 1978 when two young men attempt a picnic and boat ride, only to be thwarted by a dog who eats their food. He is noted for minor roles in Fame, Café Flesh, Night Shift, Scarface, “Girl 6”, and Fletch Lives. He appeared in the music videos for the Mike + The Mechanics song "Taken In", the Pat Benatar song "Le Bel Age", and the Kansas song "Can't Cry Anymore" all of which were made by Flattery Yukich Inc (Producer Paul Flattery and Director Jim Yukich). He appeared in A Very Brady Sequel as an LAPD detective.
In addition to his film career, Belzer was a featured player on the National Lampoon Radio Hour with co-stars John Belushi, Chevy Chase, Bill Murray, Gilda Radner, and Harold Ramis, a half-hour comedy program aired on 600 plus U.S. stations from 1973 to 1975. Several of his sketches were released on National Lampoon albums, drawn from the Radio Hour, including several bits in which he portrayed a pithy call-in talk show host named "Dick Ballantine".

In the late 1970s, he co-hosted Brink & Belzer on WNBC radio (660 AM) in New York City. He was a frequent guest on The Howard Stern Show. Following the departure of Randi Rhodes from Air America Radio, Belzer guest-hosted the afternoon program on the network.

Belzer was a regular guest on the right-wing radio show of Alex Jones and appeared on the episode covering the Boston Marathon bombing, in which he referred to the bombing as a false flag event.
In the 1980s, Belzer was a regular on Alan Thicke's short-lived show Thicke of the Night. He also briefly starred in The Richard Belzer Show on Cinemax, and hosted the Lifetime cable TV talk show, Hot Properties. By the 1990s, he was appearing frequently on television. He was a regular on The Flash as a news anchor and reporter. In several episodes of Lois & Clark: The New Adventures of Superman, he played Inspector William Henderson.

He followed that with starring roles on the Baltimore-based Homicide: Life on the Street (1993–1999) and the New York City-based Law & Order: Special Victims Unit (1999–2013), portraying police detective John Munch in both series. Barry Levinson, Executive Producer of Homicide, said Belzer was a "lousy actor" in audition when he read lines from the script for "Gone for Goode", the first episode in the series. Levinson asked Belzer to take time to reread and practice the material, then read it again. At his second reading, Levinson said Belzer was "still terrible", but that the actor eventually found confidence in his performance.

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Belzer's first two marriages were to Gail Susan Ross (1966–1972) and boutique manager Dalia Danoch (1976 – c. 1978), both of which ended in divorce. In 1981, in Los Angeles, he met 32-year-old Harlee McBride, a divorcée with two daughters, Bree Benton and Jessica. McBride, who had been seen in Playboy magazine four years earlier in that year's sex-in-cinema feature, in conjunction with Young Lady Chatterley, was appearing in TV commercials for Ford and acting in free theater when she met Belzer at the suggestion of a friend. The two married in 1985 and had a home in Bozouls, France.

Belzer survived testicular cancer in 1983. His 1997 HBO special and comedy CD Another Lone Nut pokes fun at this medical incident, as well as his status as a well-known conspiracy theorist.

On March 27, 1985, four days before the first WrestleMania, Belzer repeatedly requested on his TV talk show Hot Properties that professional wrestler Hulk Hogan demonstrate a wrestling move. Hogan applied a front facelock, which caused Belzer to pass out, and he hit the back of his head on the floor when released. After waking up, Belzer was dazed, lacerated and briefly hospitalized. He later sued Hogan for $5 million and settled out of court for $400,000 in 1990. Belzer refers to the settlement in his 1997 HBO stand-up special Another Lone Nut, revealing it helped him pay for a home in Beaulieu-sur-Mer called the "Chez Hogan" or "Hulk Hogan Estate".

Belzer's father and brother both died by suicide, in 1968 and 2014, respectively. His cousin is actor Henry Winkler.

On February 19, 2023, Belzer died from complications of respiratory disease in Bozouls, France at the age of 78.

Many paid tribute to Belzer including Christopher Meloni, Mariska Hargitay, Ice-T, and Dick Wolf.