In a night where the Roush Fenway Fords looked to be the class of the field, Kenseth made the most of his Fusion, timed his strategy and his moves to perfection, overtaking Busch following a late restart after the Joe Gibbs Racing had paced the field for 110 consecutive laps.
Once on clean air Kenseth was able to open a gap and then keep Busch on his mirrors, hoping the race would go green all the way to the checkered flag.
However with 18 laps remaining the caution waved after Johnson got loose while trying to overtake Ryan Newman for seventh place into turn one. The #48 car drifted towards the inside of the track but Johnson couldn't avoid his car then turning right, up into the banking and straight into the wall at speed.
The massive impact from which he was able to walk away unhurt brought Johnson's day to a sudden end while seriously hitting his points tally in the play-off ranking after he was classified 34th.
On the final restart, 12 laps from the end, Kenseth was able to pull clear of Busch and fend him off, putting things right after he had slipped back in a previous restart against the Joe Gibbs Racing driver while lining up beside him.
Kenseth's win vaults him up to third in the standings, while his team-mate Carl Edwards continues to lead the Chase trailed by Richard Childress Racing's Kevin Harvick by five points.
"It was an awesome win for us," said Kenseth. "I knew we had a car that if we could get it to the front it would be hard to beat. But it was really hard to pass tonight, specially after you had 20 laps or more on your tyres, you needed to get it done right away.
"It was a fun race with Kyle. We had a pretty decent restart there in the second-to-last one, got by Denny [Hamlin] and Carl [Edwards]. After running Kyle down it was tough to get by him. Glad we could make it happen because it was challenging."
Kenseth's and Johnson's race had looked almost equally promising earlier while they run first and second before a caution ahead of the halfway point shuffled the order as tyre strategies came into play.
Both of them took on a full set of Goodyear's while a number of drivers led by Tony Stewart took only right-sides, but despite being on equal footing, Johnson struggled to make as much progress as his Roush Fenway rival in the end, the Hendrick driver only racing back to the top 10 again shorty before his incident.
"The #39 just got tight on my right rear quarter panel getting in to turn one and just took the air off the side of my car and around I went," said Johnson. "From there I was trying to save the slide, got pointed back to the fence and hammered the wall."
In a day when overtaking was at a premium as proved by Johnson's incident, the younger of the Busch brothers made impressive progress after being forced to start from the back of the field following an engine change.
Busch lamented having lost a possible win, although his second place allows him to move back up to fourth in the title race.
"That 17 [Matt Kenseth] -- he found something that none of us could find tonight and made something out of nothing," said Busch. "He just out drove me. Great run by the [team]. The guys did a great job and gave me a great car. Best run we've had here in a while. Still coming up short."
Edwards extended his impressive top-10 run of results in the Chase with a third-place finish ahead of Red Bull's Kasey Kahne who scored his third-consecutive top-5 finish in the play-off. Richard Petty's Marcos Ambrose was a surprising fifth after running towards the front of the field for most of the night as his team-mate AJ Allmendinger who was sixth behind Harvick.
Tony Stewart looked as a victory contender early on, leading the first 42 laps from pole position but didn't have as much speed in the deciding stages. A late clash with Greg Biffle cost him a few spots but he recovered most of those to finish eighth ahead of JGR's Denny Hamlin and his team-mate Ryan Newman.
Penske team-mates Kurt Busch and Brad Keselowski had both a tough night, never being in contention for a top-finish. In the end Busch salvaged a 13th place while Keselowski was the first car a lap down in 16th.
It was also a difficult night for Hendrick Motorsports as besides Johnson's accident, Dale Earnhardt Jr lost further ground in the Chase after an unscheduled green flag pitstop lost him a lap to the leaders late in the race. His team-mate Jeff Gordon spun at turn two on a restart after getting tapped by Kahne, while Mark Martin had a lengthy stoppage in the garage with mechanical issues.