The dramatic victory denied Joel Quenneville of his 700th career win and kept the second-place Flyers one point ahead of the New York Rangers - with two games in hand - in the Metropolitan Division.
Coach Craig Berube admitted he was thinking about his lineup for the shootout as Giroux took a pass from Mark Streit, streaked through the neutral zone, and took several strides before firing a shot that beat Antti Raanta to the upper left side.
"When I went on the ice, there were maybe 15 seconds left," Giroux said. "I knew there wasn't a lot of time, so I just tried to shoot as hard as I could. Didn't really aim, to be honest."
"You could tell he wanted it; he was skating pretty hard and it seems like he finds a way to get his shots through most of the time," winger Scott Hartnell said. "He just absolutely got off a rocket there, and the goalie didn't even know it went in. He went down and it was already by him."
The Flyers have won three straight, including consecutive weekend victories over the Penguins.
Brayden Schenn appeared to score on a rebound with 6 minutes, 12 seconds remaining in the third period, but the goal was waved off because Vinny Lecavalier deflected the puck with a high stick before Raanta, Chicago's backup goalie, made the initial save.
The high-stick violation is not reviewable.
Raanta was brilliant in a Flyers-dominated third period, making 14 saves, including a stop on Lecavalier's breakaway with about 71/2 minutes to go.
With 1:27 left in regulation, Raanta turned aside Hartnell's shot, and Steve Downie's backhander of a bouncing puck went just wide.
The Flyers hit the goalpost twice during a third-period power play (Giroux, Jake Voracek) and twice on a first-period power play (Giroux, Mark Streit).
Trailing by 2-0 after the first 3:51, the Flyers dominated the rest of the opening period and tied the score on a pair of Hartnell goals - one that deflected off a Blackhawk, the other after he took a crafty pass from Giroux.
"The way we started, to be at 2-2 was huge," Hartnell said.
Saying he wanted to give workhorse goalie Steve Mason a rest after eight straight starts, Berube surprisingly went with Ray Emery, who hadn't played since suffering a groin injury in a Feb. 27 relief role against San Jose.
Emery made his first start since Feb. 8 and looked rusty at the outset, allowing two goals on the first four shots, including a drive by defenseman Duncan Keith that went between his legs and trickled into the net. That gave the Blackhawks eight goals on 22 shots in about 44 minutes against their ex-teammate this season.
But Emery steadied himself and made 21 straight stops after allowing the early goals, including a point-blank save on Brent Seabrook with about seven minutes left in the second period.
"I thought he read his old teammates very well," Berube said. "They had some wraparounds and he was ready for it. He stayed composed even though we were down 2-0 right away."
The Flyers hosted the Blackhawks for just the second time since Chicago won the 2010 Stanley Cup at the Wells Fargo Center.
Aside from that monumental victory, the Blackhawks have lost 12 straight in Philadelphia, including 10 in the regular season, since 1996.
The Flyers began the night in second place in the tightly contested Metro.
"We're fighting for the playoffs now," Hartnell said. "If you can't get up for these games, there's something missing in your heart."