A first-half goal from Takuma Asano and a wonderstrike from Yosuke Ideguchi settled the crucial Group B contest and guaranteed a place in Russia next year for the Samurai Blue, with one game left to play.
With Japan meeting Saudi Arabia in the final round of fixtures and Bert van Marwijk's side having suffered a surprise defeat to UAE on Tuesday, Australia knew that a win at Saitama Stadium 2002 would have been enough to seal an automatic qualifying spot of their own.
Head coach Ange Postecoglou kept faith with a more attacking-looking back-three system but chances were few and far between in a nervy encounter between two giants of the Asian section.
It was Asano, handed a starting spot ahead of the likes of Shinji Kagawa and Keisuke Honda, who kept his cool with a neat volley towards the end of the first half before Ideguchi made the win safe for Vahid Halilhodzic's side.
They now head into next week's trip to Saudi Arabia with their World Cup spot assured, while the Socceroos – level on 16 points but two goals behind the Saudis – must hope for a favour from Japan and a big win of their own over Thailand.
It was Japan who looked the more likely to break the deadlock during anxious early exchanges, with Takashi Inui firing narrowly wide of Mat Ryan's right-hand post before Asano clipped the woodwork with a header from a tight angle.
Asano just failed to reach a Yuto Nagatomo cross at the far post but Mathew Leckie came within inches of the opener, controlling Massimo Luongo's lay-off before sending a deflected effort off the base of the left-hand post from the edge of the area.
Japan's superior possession had yielded few clear chances but, with five minutes left of the half, Asano made the most of Trent Sainsbury's mistake.
Nagatomo clipped a fine delivery in from the left and Sainsbury allowed Asano to run clear towards the six-yard box and side-foot a simple volley past Ryan.
The Socceroos introduced Tomi Juric in the second half as they began to push for a way back into the contest, although Nagatomo's dipping volley following a free-kick had Ryan worried.
Veteran Tim Cahill came within inches of meeting a Robbie Kruse cut-back at the far post, with Hiroki Sakai just doing enough to put him off, as Australia began to threaten in the closing 20 minutes.
Sainsbury made a brilliant goal-line block to deny Ideguchi a second but it proved in vain for Australia, as the 21-year-old cut inside from the left before rifling an unstoppable shot past Ryan and into the top corner from 20 yards out in the closing minutes.