The 31-year-old American carded a final round 69 to finish on four under 276, eventually three shots clear of veteran Jim Furyk, who closed with a superb 66, Scott Piercy and Ireland's Shane Lowry.
He had finally triumphed after a string of near misses, most recently at last year's U.S. Open at Chambers Bay where he three-putted from short range on the 18th hole to hand victory to Jordan Spieth.
But the real drama focused on a possible one-shot penalty for an infraction on the fifth green where the ball moved on the super fast surface as he addressed it to putt.
Johnson was only told he might be penalized on the 12th tee and appeared unsettled, dropping a shot on the 14th before bravely regaining his composure under enormous pressure.
The incident revived memories of another controversial incident at the 2010 PGA Championship at Whistling Straits where Johnson was given a penalty for grounding his club in what was ruled to be a bunker, ruining his victory chances.
While he played on and with Johnson facing a video review of the evidence at the end of the round, he was backed up by other golfing stars on social media.
"This is ridiculous... No penalty whatsoever for DJ. Let the guy play without this crap in his head. Amateur hour from @USGA," tweeted Rory McIlroy, who missed the cut at Oakmont.
Spieth added: "Lemme get this straight.. DJ doesn't address it. It's ruled that he didn't cause it to move. Now you tell him he may have? Now? This a joke?"
Johnson had also found support from last day playing partner Lee Westwood at the time of the original incident and as the drama unfolded with the Englishman already out of contention.
Earlier Sunday, Lowry had taken a four-shot lead as the leaders completed their third rounds in the weather-disrupted tournament.
He closed out a magnificent five-under 65 to close on seven under with Johnson and unheralded American Andrew Landry his nearest challengers.
But that lead had gone as he played the back nine of the final round, with Johnson charging to the turn in 33 to reach five under while Lowry saw shots go to par as he struggled to find his imperious form of the morning.
Then came the drama of the possible penalty ruling, which also appeared to unsettle the other contenders after they were informed by U.S Golf Association officials.
One by one they fell out of contention to leave Johnson with a then three-shot cushion as he played the last, victory all but assured despite the possible penalty.
He duly produced two magnificent shots to leave himself a short birdie putt and with it victory.
Johnson was subsequently penalized one-shot for the incident on the fifth green, but by then it mattered little as he was left to celebrate with his fiancee Paulina Gretzky, the daughter of NHL great Wayne, and their young son Tatum.
Given the leaderboard after the third round, it was always likely a new major winner would be crowned, but world number one Jason Day briefly looked to gatecrash the party when he picked up three shots in two holes to go to one under.
But pressing for a further birdie, he found two bunkers on the 17th and his challenge was over.
Defending champion Spieth was never a factor on the Sunday, finishing nine over, while McIlroy had already exited the second major of the season.