With the referee playing a major role in a gripping encounter at Brisbane's Suncorp Stadium, both teams finished with 10 men and a goal apiece
Japan looked certain to go three wins from three matches and well on their way to Brazil when Yuzo Kurihara netted from close range five minutes after Saudi Arabian referee Khalil Al Ghamdi handed Mark Milligan his second yellow card.
However Al Ghamdi intervened again on 70 minutes, awarding a penalty against Atsuto Uchida for holding striker Alex Brosque as the Socceroos threatened from a corner.
Wilkshire stepped up and buried the penalty hard and straight to rescue a result that seemed so unlikely minutes earlier.
The Dinamo Moscow man almost stole victory in stoppage time with a free kick from 30-metres out - only the desperate fingertips of Japan keeper Eiji Kawashima ensured the stalemate.
The Samurai Blue dazzled the Socceroos for much of the match and finally found the net in the 65th minute when Keisuke Honda danced along the by-line and passed across goal for Kurihara, who made no mistake and sent the Japan's players and fans into raptures.
Japan had one last chance to steal victory when Honda lined up a free-kick 30-metres from goal, but Al Ghamdi halted proceedings, blowing the full time whistle as the CSKA Moscow man prepared to strike.
A draw was a fitting result for Australia, who dominated early without converting, before hanging on as Japan ran riot with precision passing and persistence.
Tim Cahill was reinstated to the starting side at the expense of Harry Kewell and made a marked difference early, as the Socceroos delivered on their promise to attack from the outset.
There was plenty of intent and physicality from the home side early but the Samurai Blue was unfazed and continued to go about its business in classy fashion.
Mark Bresciano was instrumental in getting the Socceroos on the attack and helped get David Carney and Carl Valeri good looks at goal from the top of the box, but both men missed the target.
The Socceroos initial onslaught was interrupted when Bresciano came from the field in the 13th minute with an apparent groin injury, replaced by Milligan.
Japan held their nerve and slowly but surely wrested momentum of what turned out to be a high-class, fast-paced encounter.
The deft midfield work of Honda and Sir Alex Ferguson’s latest acquisition Shinji Kagawa was breathtaking at times and deserved to be rewarded - and almost was when the pair combined only for Honda to fire straight into the waiting arms of Mark Schwarzer.
In the 19th minute, only a remarkable clearance from Kurihara stopped the Socceroos from grabbing a decisive goal.
Cahill, Lucas Neill and Brosque all had a chance to bury the ball into the net in quick succession inside the box, before Kurihari - laying on his back after the melee in front of goal - miraculously cleared over the crossbar.
As the half wore on, the momentum clearly moved in favour of the visitors, but their execution in front of goal let them down.
Kagawa, with Honda as his offsider, was running riot for the Samurai but could not find the back of the net, and at half-time Australia had five shots on target to Japan's one.