In the middle of the 1971-1972 season, Cherry became the coach of the AHL's Rochester Americans. After a successful three-year stint in Rochester, he was promoted to the NHL to coach the Bruins. He quickly developed a reputation for being an eccentric, flamboyant coach who pressured his players to get physical. It has been alleged he modeled the Bruins' playing style after that of his dog, Blue. The approach worked as the Bruins were one of the NHL's best teams during the latter half of the 1970s, although they did not win a Stanley Cup under his leadership. Cherry won the Jack Adams Award as NHL coach of the year in 1976.
Cherry was fired by the Bruins after a critical coaching mistake during a 1979 playoff series against the Montreal Canadiens. Up by a goal with less than two minutes left in the seventh game, he let too many men on the ice while making a line change. The Canadiens scored the tying goal on the subsequent powerplay and won in overtime.
Cherry went on to coach the Colorado Rockies the following season, but was unceremoniously dumped after one year.
He then turned his eyes to broadcasting, landing a job as a commentator on Hockey Night In Canada on the Canadian Broadcasting Corporation. Since the mid-1980s he has regularly appeared in a segment in the first intermission titled "Coach's Corner". He has become well known for his unique clothing choices (pinstripe or plaid suits and gold ties for example), his dislike of the European style of hockey, catchphrases like "You kids out there..." and overall political incorrectness.
In 2003 Cherry made controversial comments on his CBC segment in support of the U.S. war on Iraq. On an American radio program the following week, he lashed out at CBC management for being too anti-American.
Cherry was formerly the part-owner and coach of the Mississauga IceDogs, in the junior Ontario Hockey League. At first, he demanded that only Canadians could play on the team.