Jamie Joseph's men produced a devastating display of attacking rugby in front of a delighted home crowd at the Oita Dome, which will host five 2019 World Cup matches.
All four Japan tries came from scintillating attacking moves, with Amanaki Lelei Mafi and Kenki Fukuoka scoring in the first half before wing Lomano Lava Lemeki and fullback Kotaro Matsushima followed suit in the second.
Italy had kept themselves in the contest with tries from prop Tiziano Pasquali and number eight Abraham Jurgens Steyn to reach the halftime break trailing the world's 11th-ranked side 17-14.
However, Japan took control after the break with flyhalf Yu Tamura at the centre of everything positive for the Brave Blossoms, almost faultless with the boot and providing the vision to create the chances for both second half tries.
His cross-field kick was tapped back by hooker Shota Horie into the path of Lemeki to give Japan a 10-point lead with 20 minutes to play, before a deft grubber kick invited Matsushima to go over for the game's final points on 66 minutes.
The win is Japan's first over a top tier nation since their famous victory over South Africa in the pool stage of the 2015 World Cup and leaves Italy with just one win in their last 18 matches.
Conor O'Shea's 14th-ranked side will have a quick chance to gain revenge when the two sides meet again in Kobe on June 16.
(Reporting by Jack Tarrant; Editing by John O'Brien)
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