According to his manager, Sandy Joseph, "Walsh's tremendous body of work includes 119 feature films and more than 250 television productions." Being partially deaf in one ear and with an accent harkening from Vermont made it clear to Walsh: "I wasn't going to do Shaw and Shakespeare and Molière — my speech was simply too bad." His persona was a "mesmerising everyman and an indelible gargoyle" who featured "poached-egg eyes."

Walsh specialized in playing villains who were blissfully oblivious to their villainy. He brought a "delightfully menacing presence" to his characters. He was a no-nonsense worker bee in the film industry. Walsh characterized himself as approaching "each job thinking it might be my last, so it better be the best work possible. I want to be remembered as a working actor. I'm being paid for what I'd do for nothing."

Walsh spent years honing his craft in movie bit parts and on stage. After appearances in the films Midnight Cowboy (1969), Alice's Restaurant (1969), Little Big Man (1970), Escape from the Planet of the Apes (1971), They Might Be Giants (1971), What's Up, Doc? (1972), Serpico (1973), The Gambler (1974), Bound for Glory (1976), and Airport '77 (1977), Walsh came to prominence in the iconic 1977 hockey comedy film Slap Shot, in which he played the cynical small town sportswriter Dickie Dunn, and the 1978 crime film Straight Time, in which he played a vicious parole officer opposite Dustin Hoffman. USA Today film critic Mike Clark wrote that the film character who was "a cesspool in a flowered shirt" was typically Walsh. He also had a small but memorable role as a crazed sniper in the Steve Martin comedy The Jerk (1979), followed by roles in the drama films Brubaker (1980), Ordinary People (1980), and Reds (1981).
One of his best-known roles was Captain Harry Bryant in Ridley Scott's cult film Blade Runner (1982). He characterized Blade Runner as being especially difficult and tiresome to make, given director Ridley Scott's insistence on perfection. As a hard-bitten police commander, Walsh's character brings Deckard (Harrison Ford) out of retirement to "retire" cyborgs, telling Deckard, "I need your magic." Walsh allowed that he was completely confused as Blade Runner was filmed, and did not have any idea where it was going.

In 1983, Walsh appeared in Mike Nichols' biographical film Silkwood. In 1984, he was cast as a crooked Texas private eye in the film noir Blood Simple, which was the Coen brothers' first film and resulted in Walsh winning the first Independent Spirit Award for Best Male Lead. Pauline Kael praised Walsh's performance: "his broad buffoonery helps to ground the picture, to keep it jaundiced and low-down." He then reteamed with the Coen brothers for Raising Arizona as a memorable "yakking m…

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Critic Nicolas Rapold called Walsh "a consummate old pro of the second-banana business", while Roger Ebert hailed him as "the poet of sleaze". Ebert also fabricated his "Stanton-Walsh Rule": "No movie featuring either Harry Dean Stanton or M. Emmet Walsh in a supporting role can be altogether bad." Walsh was "ham-faced, heavyset" and "often played good old boys with bad intentions".

In 2018, Walsh was inducted into the Character Actor Hall of Fame by his Blade Runner co-star Harrison Ford. Later in the same ceremony he received the Chairman's Lifetime Achievement award.

Walsh had a reputation for generosity and wry wit. He habitually distributed two-dollar bills to the set's crew, with some advice: "Don't spend it, and you'll never be broke."

Walsh died of cardiac arrest at Northwestern Medical Center in St. Albans, Vermont, on March 19, 2024, three days before his 89th birthday.