Playing for the injured Michael Vick, Johnson completed 19 of 25 passes for 257 yards, leading the Falcons (2-3) to their second win of the season. Their first two losses came by a total of four points.
"I think anytime that you've been somehwere, it's special when you come back," said Atlanta Coach Dan Reeves, who guided the Giants from 1993-96. "We just needed a win, it didn't matter where we were playing."
The Falcons grabbed the lead following New York's first turnover in the fourth quarter as Johnson threw a 14-yard touchdown pass to Brian Finneran. The win was sealed when the Giants turned the ball over again in the final minutes.
"We did things that cost us football games," Reeves said of the team's 1-3 start. "And I thought today we made plays that helped us win the game. So I was really pleased."
Kerry Collins threw an interception at Atlanta's seven-yard line on the first drive of the fourth quarter and Ron Dixon fumbled in the red zone with 3:22 remaining, costing New York (3-3) a chance to enter the bye week on a high note.
A win would have given the Giants a 4-2 record. Not much was expected from a team that missed the playoffs last season, but they got off to a 2-1 start with winnable games against Arizona, Dallas and Atlanta to follow, only to lose two of them.
"In this league you can't think like that," said Giants Coach Jim Fassel, whose team suffered a handful of injuries, including a season-ending ruptured Achilles to defensive tackle Keith Hamilton.
With Vick -- Atlanta's franchise quarterback -- out with a shoulder injury, it appeared the Giants were in position for a victory. But Johnson was sharp the entire way.
Johnson also ran for a touchdown, opening the scoring 11 seconds into the second quarter with a 15-yard dash. He faked Giants defensive back Jason Sehorn into leaving his feet before finding the right side of the end zone.
"I was able to get out to my right and it opened up," said Johnson, who signed as a rookie free agent out of Florida in 2000. "That is what you hope for because when you get in a position like that, the defense is vulnerable. Then it becomes a sandlot play."
The 17-play drive took 9 1/2 minutes and chewed up 88 yards. It also forced three Giants defenders to the sidelines, including Hamilton. Michael Strahan, the NFL's single-season sack record-holder, and cornerback Omar Stoutmire also left during the drive, although both returned later in the game.
Despite being shorthanded on the defensive end, the Giants tied the game at 10-10 with 8:10 left in the third quarter when Collins found Ike Hilliard with an 18-yard strike. The 12-play, 70-yard drive appeared to swing the momentum in New York's favor.
But Juran Bolden -- a six-year veteran -- came up with his first career interception 3:21 into the fourth quarter, stalling a New York drive deep in Atlanta territory.
"Everybody was behind me. They said, 'You have to step up and make a play,'" said Bolden, who stepped in front of a pass intended for Hilliard. "It's a long game. I saw an opportunity to make a play.
"Unfortunately, I don't remember what happened after that. I got a real good knock in the head."
A six-play, 94-yard drive followed that gave the Falcons the lead for good. The second play was a 63-yard connection between Johnson and Shawn Jefferson that put Atlanta at the Giants' 25.
The final two plays went to Finneran -- an 11-yard pass and a 14-yarder into the end zone.
"His confidence is going to be a lot better," Finneran said. "But also the team's confidence in him is going to be a lot better."
The Giants still had a chance at the tying score, but safety Henry Jones stripped Dixon and Kevin Mathis recovered at Atlanta's 15.
"What can you say about those things?" Collins said. "The guy is trying to make a play, he's going down and gets stripped."
The Falcons got the ball with 3:22 remaining and used all but 18 seconds of the clock as they hit the .500 mark with their first road win in two tries this season. They host Carolina next week.
"It's a huge win," Johnson said. "We can get to 3-3 next week, and that puts us right back in the ballgame."