Miller made 15 of his season-high 31 saves in the third period, and the Vancouver Canucks scored three times in the final 15:06 of the game to beat the Blues 4-1.
"It was one I was actually really looking forward to, especially here in St. Louis," Miller said. "It was fun."
Nick Bonino, Linden Vey and Jannik Hansen broke open a tight game, scoring goals in the third period to help the Canucks (4-2-0, 8 points) snap a two-game losing streak. That made a winner of Miller, who signed a three-year, $18 million contract with Vancouver after the Blues opted not to re-sign him in the off-season.
"We didn't get the job done, and I'm going to feel really bad about that for a long time," Miller said of his time with the Blues. "But I'm going to continue to push in my career and this is where I ended up, and I'm happy to be a Canuck."
The Blues fell to 2-3-1 with their second consecutive loss.
The Canucks scored just 41 seconds into the first period off a Blues turnover in the neutral zone. Alexandre Burrows' wrist shot from the left circle was knocked down by goalie Jake Allen, but Chris Higgins was there to put home the rebound for his second goal of the season.
The Blues tied the score with a power-play goal from Kevin Shattenkirk, off assists by David Backes and Alexander Steen, with 12:22 left in the second period after the Canucks were called for too many men on the ice.
Bonino put the Canucks ahead to stay with 15:06 remaining in the third period when he scored on an odd-man rush following a Miller save of a Jori Lehtera scoring chance at the other end.
"The save he made in the third was the game," Vancouver coach Willie Desjardins said of Miller's stop on Lehtera. "If they score there, it's 2-1 them. He made the big save, we went down and scored and that changed the game."
Vey scored on the power play with 8:03 remaining, assisted by Henrik Sedin and Radim Vrbata, and Hansen added an unassisted, empty-net goal with 3:01 left.
Bonino, Burrows and Higgins each finished with two points.
"It's good to get that one, especially for Millsy," Bonino said. "He made some huge saves in the third and the second, so we're happy to win it for him."
Miller, who had allowed five goals on 13 shots in a loss to the Stars on Tuesday, came up big in the clutch on Thursday.
The Blues acquired Miller from the Sabres before the trade deadline last season, but after winning seven of his first eight starts he struggled down the stretch and posted an .897 save percentage in the six-game, first-round Stanley Cup playoff series loss to the Blackhawks.
"Listen, things didn't work out here, but he's still Ryan Miller," Shattenkirk said. "We don't forget that. He's still a great goalie and one of the great goalies in this league, so he's a hard guy to beat. Playing the way we did tonight, we had some good chances. We just have to put some more by him."
NOTES: The Canucks recorded 23 blocked shots, including five from Luca Sbisa and four apiece from Christopher Tanev and Alexander Edler. . Thursday's game was the 500th for Edler, a Canucks defenceman, and the 200th in the career of Blues forward Ryan Reaves. . There was a delay with 12:02 remaining in the first period when a piece of glass behind the Canucks goal had to be replaced. . The Blues played their second straight game without injured centre Paul Stastny (upper body injury). . Lehtera won 11 of his 14 face-off attempts Thursday.