Johnson lost a three shot lead at the second hole to blow the final round at Pebble Beach wide open, and playing partner McDowell was rising to the challenge as some of golf's biggest names faltered.
American Johnson, 25, did not last long with the pressure of a Sunday lead at the Majors, leaving Northern Ireland's McDowell in the lead at three under par after nine holes, two ahead of France's Gregory Havret, following the day's early drama.
Johnson had gone into the final round with a seemingly unflappable demeanour as he sought to protect his lead at six under par and win his first Major.
Rejoining battle with halfway leader McDowell for the second day in a row, having outscored him by five shots in the third round, Johnson walked off the par four second hole in a tie for the lead at three under after a terrible triple bogey seven and then lost his ball off the third tee in a nightmare series of events for the World Number 29.
Johnson had found the top of a greenside bunker with his second shot on a hole that is normally designated a par five. He played left-handed from there and fluffed that third shot, then needed two more to get out of greenside rough before two-putting as Northern Ireland's McDowell parred his first two holes.
There was further trouble for Johnson when he strayed off the next tee, losing his ball in thick rough to the left of the third fairway on the par four hole and having to return to the tee after using up his allocated five minutes to find it on the way to a double bogey.
Having been made to wait, McDowell, the leading putter in the tournament so far, had done well to sink a far from easy par putt and the 30 year old from Portrush went to the fourth having regained the lead at three under as Johnson slipped to one under.
Johnson was all at sea, figuratively and literally at the fourth as his tee shot rolled over the edge of the cliff and after taking a drop, he missed his par putt from five feet to fall further behind.
But while the American faltered, McDowell was rock solid and when he did eventually drop a shot at the par four ninth, he became the last player in the field to bogey on the final day.
Another followed at the tenth but South Africa's Ernie Els, a two-time US Open Championship winner who had shared the lead with McDowell at three under after his first six holes, was also finding trouble.
Els double-bogeyed the long ninth hole, sending his second shot into right rough on a steep slope between fairway and beach, and then bogeyed the tenth to return to his starting point at level par.
Having birdied the first and sixth holes, Havret wobbled too, bogeying the eighth and tenth to fall back to level par alongside Els.
Tiger Woods, Havret's playing partner, had launched his bid for a 15th Major from five strokes back of the lead having shot a five under par 66 on Saturday to reach one under par.
However, the World Number One, who won the 2000 US Open Championship on its last visit to Pebble Beach by a Majors record 15 strokes, could not maintain the brilliance of the previous night, when he scorched through the back nine with five birdies.
He bogeyed the first after missing a short putt, scrambled a saved par at the third thanks to an excellent second shot from thick rough in a wooded hollow beneath the fairway but then bogeyed the fourth before emulating Johnson and going over the cliffs - this time at six - and then bogeying nine, leaving him three over with seven to play.
Masters Tournament champion Phil Mickelson had birdied the first to reach level par but the World Number Two then three-putted the fourth having driven the green and, like playing partner Els, came undone at the ninth with a bogey to stand at one over with five to play.