Two former Oilers, Dean McAmmond and Mike Comrie, scored in the shootout, and Mike Fisher had a goal and assist in regulation, to lead the Senators to a 4-3 win over the Oilers and give Murray his 600th career coaching victory. Murray, 64, becomes the fifth NHL coach with 600 wins behind Scotty Bowman, Al Arbour, Dick Irvin and Pat Quinn.
"It's elite company, no question about it, and I respect it a great deal," said the Shawville, Que., native who earned the milestone in his 1,199th career game after winning his first back on Nov. 14, 1981 as coach of the Washington Capitals.
"To win that many games it's a great compliment to the players I've had, to the teams I've coached," Murray said.
The milestone was nearly missed as Oilers winger Petr Sykora scored twice in a 14-minute span of the third period to erase a 2-0 deficit before rookie defenceman Tom Gilbert scored his first NHL goal in his third career game. That goal forced overtime with 19.9 seconds left in regulation.
"Definitely an unbelievable feeling," said Gilbert. "Our mentality was never quit."
Comrie, an Edmonton native, acquired by the Senators in a Jan. 3 trade with Phoenix, began his career in Edmonton. He fell out of favour in the Alberta capital and was traded after a lengthy and bitter contract dispute.
On Tuesday he was a hero again.
"It was a feeling of relief," said Comrie, who scored the shootout winner, but was still booed by pockets of Oilers faithful. "I was happy to be able to contribute."
The loss stretches the Oilers winless streak to four on their seven-game road trip.
"It was kind of fitting it went into overtime," said Senators captain Daniel Alfredsson, who also scored in regulation after dancing through a bewildered Oilers defence off a feed from Fisher before tucking his 20th goal of the season behind a falling Markkanen at 12:17 of the third period.
Alfredsson, who recorded his ninth season of 20 goals or more, took a shot at Murray following the historic win.
"It means he is very old," the Ottawa captain joked. "It's nice for him to do this at home."
Martin Gerber stopped 27 shots for his sixth straight win and third in relief of Ray Emery, the Senators No. 1 goalie, who served the last of a three-game suspension after slashing Montreal's Maxim Lapierre on Feb. 10.
Trailing 2-0 to open the third period, Sykora beat Gerber to his blocker side with a long slap-shot on a power-play at 1:34. The Czech winger then intercepted a clearing attempt from Senators centre Chris Kelly and snapped a shot past a stunned Gerber at 15:48 to close the Senators' lead to 3-2. Gerber, who improved to 11-9-1, held on to win for the first time in four career starts against the Oilers.
Fisher ran his point streak to six straight games after slinking into the high slot and going untouched before snapping a shot over the glove of Markkanen for a 2-0 lead in the second period.
Markkanen faltered on the play, but was elastic at times finishing with 31 saves after his first start in nine games in relief of Dwayne Roloson.
"Hopefully we can build from this game and get some momentum," said Oilers captain Jason Smith.
Heatley opened the scoring with his 33rd goal on the Senators 12th shot at 14:44 of the first period, beating Markkanen with a low shot to the glove side.
The teams combined for 25 hits and 19 shots after a feverish and physical opening 20 minutes.
Edmonton, which fell to 0-3-1 after the fourth of a season-high seven-game road trip, appeared in Ottawa for its first game since battling the Senators to a 3-3 tie on Nov. 6, 2003.
Ottawa is in Buffalo to begin a home-and-home series with the Eastern Conference-leading Sabres on Thursday, while the Oilers are in Columbus.
Notes: Sykora has 33 career two-goal games but no career hat-tricks ... Murray, without a contract for 2007-08, remains the longest
serving NHL coach not to win the Stanley Cup... The Oilers scratched defenceman Matt Greene and forwards Zach Stortini and Petr Nedved.