Ruff was chosen in the second round, 32nd overall of the 1979 NHL Entry Draft. He played for the Buffalo Sabres and New York Rangers. Ruff gained a reputation as a player for his toughness, character and hard work on the ice. An illustration of this came in a May 10, 1980 playoff game against the New York Islanders where opposing goaltender Billy Smith struck Ruff with his stick as he passed in front of his net. Ruff got up, skated back to the goaltender and tackled him.
Ruff played most of his NHL career for the Sabres, serving as captain of the team for nearly three years, but he was traded to the Rangers at the 1989 NHL trade deadline in exchange for a draft pick. The Sabres would use that pick to select Richard Smehlik, who would later play for several years under Ruff.
Ruff played in 691 NHL games, scoring 105 goals and adding 195 assists for an even total of 300 points. He also recorded 1,264 penalty minutes. In 52 playoff games, Ruff recorded 11 goals and 13 assists while accumulating 193 penalty minutes.
He became assistant coach of the Florida Panthers for the 1993–94 NHL season until the 1996–97 NHL season. His most success as an assistant coach was with the 1996 Florida Panthers that made it to the Stanley Cup final, but lost to the Colorado Avalanche.
Ruff was named the 15th head coach of the Buffalo Sabres on July 21, 1997. He joined a long list of former Sabres players who eventually became Sabres head coaches; Floyd Smith, Bill Inglis, Craig Ramsay, Jim Schoenfeld, and Rick Dudley were among the others. He had immediate success in Buffalo, advancing to the Eastern Conference Finals in the 1997–98 NHL season. In Ruff's second season as coach, the Sabres reached the 1999 Stanley Cup Finals before finally losing to the Dallas Stars in six games. The Stars' Brett Hull scored a goal deep into the third overtime. There was a dispute that Hull's skate was in the goalie's crease before he had control of the puck, which was (under then 1999 rules) a clear violation, giving Dallas the Stanley Cup championship. The following two seasons saw Ruff's Sabres lose in the first round to the Philadelphia Flyers and the second round to the Pittsburgh Penguins respectively. Buffalo missed the playoffs in the three seasons preceding the NHL lockout amidst the team's bankruptcy and financial problems caused by the Adelphia Communications corporate scandal. After the lockout, Ruff lead the Sabres to back-to-back Eastern Conference Finals appearances only to lose to the Carolina Hurricanes in 2006 and the Ottawa Senators in 2007. Ruff was the longest-tenured coach in the NHL and was rewarded with a three-year contract extension that has an option for a fourth season.
Ruff is known for being blunt with the media. A well-known example of his bluntness were his comments regarding Toronto Maple Leafs player Darcy Tucker. In his post-game interview following a questionable hit on Jochen Hecht that knocked the Sabres center out of the lineup for two weeks with a sprained ACL in the 2005–06 season, Ruff said, "I want him [Tucker] suspended." He also said, "I have not called the NHL office all year and I will call them ten times tomorrow." He called Tucker's hit "a definition of a joke."
On April 5, 2006, Ruff became the 31st coach in NHL history to win 300 games, and just the 16th to do it with only one team. Ruff led the Sabres to their most successful regular season ever in 2006–2007, with a 53–22–7 record for a total of 113 points.
Ruff was the winner of the 2005–06 Jack Adams Award for coach of the year in the National Hockey League. Tom Renney of the New York Rangers and Peter Laviolette of the Carolina Hurricanes were also nominated.
Ruff was again nominated for the Jack Adams Award in 2006–07. His nomination was the second time he has been a finalist for coach of the year. Michel Therrien of the Pittsburgh Penguins was also a finalist while Alain Vigneault of the Vancouver Canucks won the honor. Ruff placed 2nd in the voting with 126 points to Vigneault's 134.
In February 2007 Ruff was fined US$10,000 by the NHL after a brawl with the Ottawa Senators (Which Buffalo Sabres fans started funding for the fine, But Lindy Ruff declined that offer). The league said that Ruff precipitated the brawl following a questionable hit on then co-captain Chris Drury by the Senators' Chris Neil. Because the hit to Drury did not result in a penalty, Ruff sent out Andrew Peters, Patrick Kaleta, and Adam Mair, the team's "enforcers". What followed was one of the '06–'07 season's most memorable hockey brawls. Adam Mair began the brawl, punching Ottawa's Jason Spezza as soon as the puck was dropped. Andrew Peters tried to start a fight with Dany Heatley, who was reluctant to respond, at one point even hiding behind a linesman. The goaltenders got into the fight, with Martin Biron challenging Ray Emery, and Ruff himself engaged in a prolonged shouting match with Senators coach Bryan Murray.
After a second round playoff match against the New York Rangers on April 27, 2007, Ruff would be fined again by the league after harshly criticizing officials for an alleged missed too-many-men call against the Rangers, which might have given Buffalo a chance to tie the match in the closing minute.
In the 2006–07 season he became the first Sabres coach to lead the team to back-to-back 50 win seasons, boasting the 5th best points percentage in the league since 1979.
On October 15, 2008, Ruff became the 23rd coach in NHL history to win 400 games, and just the 7th to win 400 games for one team.
Ruff was named as an associate coach for Team Canada, which won the gold medal at the 2010 Olympics in Vancouver.
On January 6, 2011, Ruff became only the 16th coach in NHL history to win 500 games, and just the 2nd to win 500 games while only having coached one team.
On January 8, 2011, Ruff became the winningest coach who only coached for one team in NHL history when the Buffalo Sabres defeated the Phoenix Coyotes 2–1 in overtime. His 501st win behind the bench with the Sabres put him one ahead of Toe Blake who coached to 500 wins with the Montreal Canadiens. Al Arbour won more games for the New York Islanders, but he also coached the St. Louis Blues early in his career. Along with Arbour, Billy Reay, and current Washington Capitals coach Barry Trotz, Ruff is one of just four coaches to coach 1,000 NHL games with a single team.
On April 29, 2011, the Sabres announced that Ruff had agreed to a multiple year contract extension.
On February 20, 2013, the Sabres announced that Ruff had been relieved of his coaching duties., ending his tenure as the NHL's longest active-serving coach with one team and second only to Gregg Popovich in the four major sports in North America. Ron Rolston, head coach of the Rochester Americans, was named as his replacement.
On June 20, 2013, the Dallas Stars announced that they were in the process of hiring Ruff as head coach. This was also on the anniversary of the controversial defeat of the Buffalo Sabres in the Stanley Cup Finals in 1999.
On June 21, 2013, the Dallas Stars announced that Ruff would be their new head coach.
He continues to support Buffalo even in his current role against them. Of late he was quoted saying, "I am saddened by the current status of the Buffalo Sabres. I am deeply disappointed in the direction the team has gone since my leaving. I wish them all the best, and hope for winning days ahead, but not tonight." This being said on his first day back to Buffalo, in which the Stars won 4-3.
In 2014 Ruff led the Stars to their first playoff appearance since 2008, but lost in the opening round to the Anaheim Ducks in six games.
Ruff's younger brother, Brent Ruff, was one of four teammates killed in a bus crash while playing for the Swift Current Broncos in 1986.
Another younger brother, Marty Ruff, was a first round draft pick of the St. Louis Blues, but never appeared in an NHL game.
An older brother, Randy Ruff, played and coached in junior hockey.
Lindy and his wife Gaye have four children: Brett, Eryn and twins Madeline and Bryan. The Ruffs primary residence is in Clarence, NY, while Lindy also has a place of residence in the Dallas-Fort Worth area where he lives during the hockey season.