Second-half tries from foreign-born players Craig Wing and Michael Broadhurst helped re-write the record books for Japan against a depleted Wales, who were missing their head coach and 15 players because of the British and Irish Lions tour.
Despite the unfamiliar Welsh line-up, the result is a boost for rugby in Japan, the hosts of the 2019 World Cup who have played in all seven editions of the tournament so far but have won only once, against minnows Zimbabwe in 1991.
"I`m very proud of the team. They have created a history today to become the first Japanese team to beat a top 10 team in the world," said Japan coach Eddie Jones.
"Obviously Wales haven`t the best 15 players, but today we played a very good game of Test rugby and it`s another step forward for the team."
Japan played their first international fixtures in the 1930s, and they first took on a Wales XV in Cardiff in 1973. In nine full Tests with Wales, Japan have been on the wrong end of some giant scores including a 98-0 blow-out in 2004.
However, steeled by last week`s narrow 22-18 defeat, Japan edged the first half 6-3 thanks to the boot of fullback Ayumu Goromaru, and after a Welsh try on 44 minutes they hit back with two of their own before wrapping up a worthy win.
"I`m very happy to play the game in front of so many people. We were really unhappy last week in Osaka, so I really wanted to live up to their expectations," said Japan`s captain Toshiaki Hirose.
"But this is only one win. I`m happy today, but I`ll continue to work hard aiming to reach top 10 in the world," he added.
In hot and humid conditions at Tokyo`s Chichibunomiya Stadium, Japan took an early lead through a Goromaru penalty but visiting flyhalf Dan Biggar levelled the scores before Welsh wing Harry Robinson came close to the opening try.
However, a long-range potshot from Goromaru six minutes before half-time gave Japan their three-point lead at the break, raising hopes of a famous win.
Wales came out firing at the start of the second half and Robinson again went close before left wing Tom Prydie finally crossed following great work from replacement back Rhys Patchell and a long pass from Biggar.
But Japan quickly regained the initiative at 13-8 when Wing, a former rugby league international for Australia, went over after steady build-up play involving a number of phases.
Wales responded by making a raft of substitutions, but they were forced into some last-ditch defending when Robinson and Liam Williams combined to halt Japanese number eight Takashi Kikutani just short of the line.
And New Zealand-born Broadhurst extended Japan`s lead when he went over in the right corner for their second try on the hour-mark, with Goromaru slotting the extras for a 20-8 lead with 20 minutes to go.
Welsh hopes took another hit when they were controversially denied a try after Patchell pounced on a grubber kick by Biggar, only to be judged not to have grounded the ball.
With three minutes left, Goromaru landed his third penalty to make sure of a win which prompted celebrations in Tokyo, and will also lift 15th-ranked Japan in their fight to join rugby`s top 10 by the next World Cup in 2015.
"We didn`t lose because of the (hot) weather. We didn`t take the chances just (because of) individual mistakes. Sometimes in rugby those things happen," said Wales captain Bradley Davies.
"Everything went wrong for us and everything went well for Japan."
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