The Dutchman, 26, started the day in fourth, 53 seconds behind leader Nairo Quintana but beat the Colombian by more than a minute on the 29.3km last stage.
Quintana, who had been chasing the first leg of a Giro-Tour de France double, had to settle for second place.
Dumoulin also leapfrogged defending champion Vincenzo Nibali and Thibaut Pinot, who dropped to third and fourth.
"It's really crazy," said Team Sunweb rider Dumoulin, who became the first Dutch winner of the Giro and the first rider from his country to win a Grand Tour since Joop Zoetemelk's victory in the 1980 Tour de France.
"This is incredible. It was such a nerve-wracking day but I had good legs and I just went for it."
Britain's Adam Yates was beaten in the race for the white jersey, awarded to the quickest rider under the age of 25, by Luxembourg's national time trial champion Bob Jungels.
Yates, 24, started the time trial with a 28-second advantage over Jungels, but the Luxembourger's time of 34 minutes two seconds was more than one minute quicker than Yates.
Jos van Emden won the stage in a time of 33:08, 15 seconds clear of Dumoulin, who crossed the line in 33:23 to claim second and he then had an agonising wait for first Pinot, then Nibali and finally Quintana to reach the finish.
Movistar's Quintana, the 2014 Giro champion, and twice winner Nibali are climbing specialists and they knew they would struggle to defend his lead on a flat route more suited to time trial specialists.
And so it proved with Dumoulin quickly erasing the advantage the riders ahead of him had after 20 stages of racing.
His winning margin is not the narrowest in Giro history, with Fiorenzo Magni winning by just 11 seconds in 1948. The closest win in Grand Tour history was Frenchman Eric Caritoux's six-second victory at the 1984 Vuelta, while Greg LeMond won the 1989 Tour de France by eight seconds.
Britain's Geraint Thomas, who was co-leader of the nine-man Team Sky squad, was forced to pull out of the race after crashing on stage nine.
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