The draw dents Japan's 100 per cent record in final qualifying, but they still top the five-team Group B on seven points from three games. Australia have two points from two games. The top two are guaranteed a Brazil 2014 berth.
Saudi referee Khalil Al Ghamdi pointed to the penalty spot and yellow carded Atsuto Uchida for pulling Alex Brosque inside the area as an Australian corner came in, and Wilkshire made no mistake in front of 40,000 in Brisbane.
The Socceroos had an early setback, losing playmaker Mark Bresciano after 13 minutes with a leg injury. He was replaced by Milligan.
The home side had a scare when Honda's shot bounced off Mark Schwarzer with Lucas Neill hacking away to safety, and moments later Shinji Okazaki's header was narrowly wide.
The Socceroos came close to opening the scoring after 19 minutes when Uchida blocked a goal-bound shot by Neill and David Carney's drive was deflected away by Kurihara.
Kurihara received his first yellow card for holding back Cahill in a centrefield sprint after the ball and Milligan joined him in the referee's book for bringing down Honda.
Milligan received his second yellow in the 55th minute for dangerous play as his outstretched foot made contact with Uchida.
The Blue Samurai piled on the pressure and they got the crucial goal in the 65th minute off a Honda pass across goal for the unmarked Kurihara to sidefoot home, before Wilkshire came to Australia's rescue.