He's taken more questions than snaps this season, and spent more time learning the complexities of the Indianapolis offense than demonstrating his skills.
Those days may be about to end.
With Indy locking up the AFC South title, a first-round bye and homefield advantage in the playoffs, Manning's playing time will likely be reduced over the next three weeks, putting Painter in the spotlight as the Colts pursue perfection.
"I won't put any added pressure on myself," Painter said Tuesday. "I don't think anything is going to change. But if I go in, I'm going to be expected to play at a high level."
It's a standard philosophy for unbeaten Indy (13-0), which has proved the mantra "next man up" can work.
Safety Melvin Bullitt has played the best football of his three-year career, replacing 2007 NFL defensive player of the year Bob Sanders.
When projected starter Anthony Gonzalez went down with a knee injury in the first quarter of Indy's season-opener, the Colts turned to rookie Austin Collie, whose 50 receptions are No. 3 on the team, and second-year receiver Pierre Garcon, who needs 251 yards to reach 1,000.
Rookie cornerbacks Jerraud Powers and Jacob Lacey rank fifth and sixth on the team in tackles after filling in for injured Kelvin Hayden and Marlin Jackson, and linebacker Philip Wheeler has done a reasonable job replacing Tyjuan Hagler, also sidelined with an injury.
But replacing Manning?
The three-time MVP has never missed a start in his 12-year career, a streak of 189 regular-season games and 15 in the postseason, and he's not likely to miss one this year, either. Coach Jim Caldwell announced this week that "healthy" starters would play Thursday night at Jacksonville, though he hasn't said whether they'll be on a play count.
If the Colts follow past trends, Manning will play briefly in the final two games before being lifted.
That would make Painter the first rookie quarterback to enter a Colts game since Jim Sorgi in 2004.
No, it's not the way Indy scripted it, but when Sorgi hurt his throwing shoulder in practice a month ago, Indy went to Plan B.
Painter was elevated to No. 2.
When Sorgi went on season-ending injured reserve last season, Painter was the only other active quarterback on Indy's roster.
"It's never good going on IR this time of year," Sorgi said dejectedly Thursday. "You got through the whole season and this is my time. But I've still got a job to do."
His task: Helping Painter, the former Purdue starter and Indiana native, prepare for his NFL debut -- whether it's this week at Jacksonville (on NFL Network) or next week in Lucas Oil Stadium against the Jets.
The longtime backup to Manning insists he can be an asset, and Painter will take all the help he can get.
"Simply having him on the sideline, whether it's practice or games is valuable for me," Painter said. "He can explain what he's doing, why he's doing it, he helps me out a lot."
So will Painter be effective when he finally makes it onto the field?
He hasn't taken a game day snap since the preseason. And while he has impressed coaches in practice and meetings, the real test will come when he starts throwing passes.
"He has certainly come along from a conceptual standpoint. He's spent a lot of time in the meeting room, preparing for each game," Caldwell said. "His grasp (of the offense) is improving, but the thing that's missing is his opportunity on the field. Until that happens, I wouldn't be able to give you a full sort of review on his progress."
The challenge isn't just filling in for Manning.
It's producing the expected results.
Painter will be asked to win games, keeping the Colts' 22-game winning streak and undefeated season intact, things few - if any - rookie quarterbacks have ever been asked to do.
"I'm confident," Painter said. "Each week, you get better and continue to learn more. You never know when it (playing) is going to happen. But there's not a whole lot of difference in preparation. You always prepare like you're going to play."
Copyright 2009 by The Associated Press