Junichi Inamoto's goal gave Japan their first World Cup finals win and blew Group H wide open.
The midfielder who has struggled to win a place in Arsenal's first-team, slotted in a 50th-minute goal to send a nation into raptures.
Japan's pacy, exuberant football proved too potent a cocktail for Russia, and Hidetoshi Nakata came close to adding a second when his shot struck the bar.
We saw a great Japanese team and our victory was fully merited
Japan coach Philippe Troussier
Inamoto stoked up the already electric atmosphere on five minutes when he strode forward to unleash a ferocious shot wide of the target.
Stand-in captain Tsuneyasu Miyamoto, sporting a black protective face mask, twice read dangerous situations to kill off dangerous through balls.
Veteran Russian sweeper Viktor Onopko - winning his 100th cap - used all his experience to cut out Inamoto's long ball which threatened to put Takayuki Suzuki clear.
The game was being played at a cracking pace and on 16 minutes, teenager Marat Izmailov had Japanese hearts in their mouths when his shot curled just wide of the post with goalkeeper Seigo Narazaki groping.
Despite the pace, two well-organised defences kept the attacks at bay, but Japan opened the Russians up on 27 minutes.
Koji Nakata outstripped Andrei Solomatin and his low cross was palmed out by Russian keeper Ruslan Nigmatullin as far as Hidetoshi Nakata who blazed over the unguarded goal from 18 yards.
Inamoto celebrates his second goal of the tournament
Japan were certainly pumped up for the occasion and Narazaki bravely plunged at the feet of Ruslan Pimenov as Yegor Titov's neat reverse-pass almost played him in.
Titov's pass inside Koji Nakata opened up Japan's defence but Kazayuki Toda read the danger superbly to slide in and divert Solomatin's cross behind for a corner.
As half-time approached Narazaki again took command of the situation as defenders in front of him hesitated, bravely plunging in to claim Yuri Nikiforov's through ball.
Valery Karpin tried to bring some cool, calm reason amidst the hurly-burly as he delicately picked his way to the by-line where his cut back was touched wide by Izmailov.