After the win, the players awarded Hartley with a fireman's helmet that usually goes to the hardest worker in the game.
"To be honest, I think I have no business with this prestigious fire helmet but at the same time, I told the players that I really respected the fact that they presented me with the helmet," said Hartley, who earned 193 of those wins when he coached Colorado from the 1998-99 season until he was let go 31 games into the 2002-03 season.
"I told them that I'm ready to trade that helmet to see them in the playoffs. I don't know where this season, this story, is going, but it's certainly fun and it's certainly very entertaining for us, the coaching staff."
Monahan scored the game winner when he picked up a rebound in front of the net and lifted it over fallen Colorado goalie Semyon Varlamov to lead the Flames (17-8-2) to their fourth straight victory.
"I cut through the middle and (Mark Giordano) made a great pass to me and got a shot on net and found a rebound," said Monahan, who was happy to score the goal to give Hartley his 400th win.
"It's well deserved. That's a big one for him. Obviously he used to be there (in Colorado). Right now we're rolling. Even as a group we knew we had to find a way to win that one."
Dennis Wideman had a pair of goals for the Flames, Curtis Glencross also scored, and Kris Russell had three assists.
"It's pretty sweet for him to get that against a team he won the Cup with back in the day," Glencross said. "I imagine it's one he'll never forget and he came in after the game and said that his 400th win wasn't as important as it is for us to get into the playoffs."
Karri Ramo made his fourth straight start in net for the Flames and finished with 21 saves to improve his record to 8-2-1.
Matt Duchene, Nick Holden and Alex Tanguay scored for the Avalanche (9-11-6), which also lost 4-3 at home to the Montreal Canadiens on Monday.
"In the third period, giveaways will always hurt you and that's what cost the second goal and the third one," said Colorado coach Patrick Roy, who played goal for the Avalanche during Colorado's Stanley Cup triumph in 2001 with Hartley as coach.
While Roy was frustrated with the overtime loss, he was pleased to see his former coach reach the 400-win mark.
"I'm happy for him, but I wish he would have done it another night," quipped Roy after the game.
Varlamov, who missed Colorado's past six games with a groin injury, made 26 saves in a losing cause.
After a scoreless first period, the Flames went up 1-0 at 2:20 of the second with a power-play goal from Wideman, who drove to the net and batted a pass from Johnny Gaudreau out of mid air and past Varlamov.
The Avs appeared to respond with a power-play goal of their own 89 seconds later, but the goal was disallowed after a lengthy review when it was determined that Daniel Brier used his left hand to bat the puck into the Calgary net.
"Certainly that PP goal would have been nice," said Tanguay, who took the initial shot. "The puck didn't look like it moved, so I don't know what they saw. It's disappointing. We keep finding ways to lose games."
Colorado kept pressing and were rewarded when Duchene finished off a give-and-go passing play with Ryan O'Reilly by snapping a shot past Ramo at 13:23 of the second.
Only 58 seconds later, the Avs took a 2-1 lead when Zach Redmond threw a pass to the front of the net that hit Calgary defenceman Ladislav Smid before bouncing off of Holden's skate and past Ramo.
Glencross scored at 1:14 of the third period when he one-timed a pass from David Jones past Varlamov.
Tanguay then put the Avs up 3-2 at 14:14 of the third when he made a nice move to get past Russell before outwaiting Ramo and wristing a shot over the Calgary goalie's blocker.
"That would have been nice to see Tangs' goal hold up," said Avalanche forward and former Flame Jarome Iginla. "That was one of the better goals I've seen in person in a number of years. It stings for us and obviously a big win for them."
Wideman sent the game to overtime when his shot from the point sneaked past Varlamov, who was screened on the play by both Jiri Hudler and Glencross.
Just seconds into the extra period, Varlamov stuck out his right pad to deny a breakaway attempt by Paul Byron.
Notes: Colorado forward Jarome Iginla returned to the Saddledome for just the second time since the Flames traded him to the Pittsburgh Penguins in March of 2013. He also played one game in Calgary with the Boston Bruins last season before he signed as a free agent with Colorado in the off-season. ... Iginla played in his 1,336th game, one behind C Adam Oates for 49th most in NHL history. … Wideman leads all NHL defencemen with 10 goals. … Calgary improved its record to 11-1-2 when scoring first.