Rolston was in his second season as coach of AHL Rochester, the Sabres' minor-league affiliate. And he has long-tenured shoes to fill in replacing Ruff, who became the franchise's winningest coach over 16 seasons.
The change comes a day after the Sabres were booed off the ice during a 2-1 loss to Winnipeg, and after Ruff had finished overseeing a 90-minute practice in preparation for Buffalo's game at Toronto on Thursday.
General manager Darcy Regier called the team's lethargic performance during the loss to the Jets as "a tipping point." And he added that discussions to fire Ruff had begun earlier in the day.
The Sabres (6-10-1) have gone 4-10-1 since opening the season winning their first two games.
Regier went to Ruff's home to inform the coach of the decision. He then allowed Ruff to visit with players as they boarded a bus to travel to Toronto.
Rolston was scheduled to arrive in Buffalo on Wednesday evening and then join Regier in traveling to Toronto for his first meeting with the team. Regier said he'll use the remainder of the season to determine whether Rolston deserves taking over the job on a full-time basis.
Before being hired by the Rochester Americans, Rolston spent seven seasons as coach of USA Hockey's National Team development program. During that time, he became the first coach to lead the U.S. Under-18 team to win three gold medals (2005, 2009, 2011).
Rolston is also familiar with numerous Sabres, including center Cody Hodgson and forward Marcus Foligno. He spent the first half of this season coaching both, as they played in Rochester during the NHL lockout.
Ruff finished with a 571-432-162 record, and was also the active leader among NHL coaches with the same team.
The news of his firing came as a surprise only because Sabres management, including team president Ted Black, had spent much of the past week voicing its support of Ruff. Team owner Terry Pegula was also regarded as a big fan of Ruff.
Pegula, however, was running out of options in his bid to turn the Sabres into a Stanley Cup contender, an objective he made clear upon purchasing the team two years ago. Ruff's firing comes nearly two years to the day Pegula formally took over as the Sabres owner on Feb. 22, 2011.
"The hockey world knows how I and the entire Buffalo Sabres organization feel about Lindy Ruff not only as a coach but also as a person," Pegula said in a statement released by the team. "His qualities have made this decision very difficult. I personally want Lindy to know that he can consider me a friend always."
Ruff was becoming increasingly aware that his job was on the line. Last week, he described the Sabres struggles as being "his mess," while adding that he wasn't done trying to clean it up.
On Wednesday, he abruptly cut short his availability with reporters by hinting that changes were coming because "it isn't working the way we're going." He didn't specify what those changes might be.
Under Ruff, the Sabres made the playoffs in each of his first four seasons and eight times overall. That included a surprising run to the Stanley Cup final in 1999, when Buffalo was eliminated by Dallas in six games.
The Sabres lost that series to the Stars on what was regarded a controversial finish. Brett Hull's decisive goal scored in a 2-1 triple-overtime win was allowed to stand despite the Stars forward having his skate in the crease, which at the time was considered illegal.
The Sabres, however, haven't been the same since they reached the Eastern Conference finals losing both times in both 2006 and '07. Buffalo has missed the playoffs in three of the past five seasons.
Last year, the Sabres were regarded as one of the NHL's biggest busts in missing the playoffs with a high-priced roster. The previous offseason, Pegula committed nearly $140 million in salary to add talent and re-sign players.
Ruff had maintained his job under three owners, and also weathered the Sabres declaring bankruptcy during the 2002-03 season before Tom Golisano purchased the team. Ruff had considered quitting his job after that season before he was talked into staying by new managing partner Larry Quinn.
The Sabres prided themselves in the stability they had at GM and coach. Regier was in his second season in Buffalo when he hired Ruff to take over after Ted Nolan declined to accept the team's one-year contract offer to re-sign.
There had been 170 coaching changes in the NHL since Ruff was hired on July 21, 1997. And among North America's four major pro sports, Ruff's tenure was second only behind Gregg Popovich, who's been coach of the NBA San Antonio Spurs since 1996.
Ruff's 571 wins rank second in the NHL with one team, trailing only Al Arbour, who had 740 wins with the New York Islanders.
Ruff's ties to Buffalo go back to his days as a player. Selected in the second round of the 1979 draft by the Sabres, Ruff made the team later that year. In November 1986, he replaced star Gilbert Perreault as the Sabres captain.