Jockey Mirco Demuro has previously won the Japan Cup and the Italian Derby
Victoire Pisa clinched the Dubai World Cup as Japan sealed an emotional one-two in 'the richest race in the world'.
The Katsuhiko Sumii-trained four-year-old, a 12-1 shot, led home Takayuki Yasuda's 40-1 outsider Transcend.
Referring to the recent disasters that have hit Japan, Sumii said: "I felt the whole country was behind me."
Monterosso, also a 40-1 shot, was third for Godolphin in the $10m (£6.2m) event but favourite Twice Over, trained by Henry Cecil, was a distant ninth.
Irish Derby winner Cape Blanco battled hard under Jamie Spencer to take fourth for trainer Aidan O'Brien.
However, the day belonged to Japan, still struggling to cope with the aftermath of the earthquake and tsunami earlier this month. Many of the owners and trainers wore polo shirts emblazoned with a message of support for those affected.
It is the first time a horse trained in Japan has won the race, which was first contested in 1996.
"I love you Japan, thank you so much," said Italian jockey Mirco Demuro after his win.
Victoire Pisa's owner Yoshimi Ichikawa receives the trophy
Trainer Sumii described victory as "unbelievable" after seeing his charge recover for a bad start to fight off Transcend having left the rest of the field around the halfway point.
Only half a length separated the pair at the post. "I didn't think we would win until the very end," Sumii said.
Twice Over had raised hopes that he might overcome being drawn in stall 12 after he seized victory from out wide in round three of the Al Maktoum Challenge earlier this month.
But despite an identical course and distance, jockey Tom Queally could not coax a similar result from his ride.
"They went very slowly early and that didn't suit him," said trainer Cecil of the 2-1 favourite.
"He broke well and was up there but couldn't get back in. The next minute they slowed it up and he got shuffled back through the field.
"He never got anywhere and it is disappointing, but that is the way it goes. It is such a shame as he was very well."