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Tommy Oar's fortuitous late strike had looked set to condemn the hosts to an undeserved defeat. But after Matthew McKay handled in the box, Honda drove his spot-kick straight down the middle to earn the necessary point.
The result left the Asian champions seven points clear and uncatchable in Group B, putting them through to their fifth straight World Cup. It is the first time they have sealed qualification on home soil.
"I was nervous. I tried to hit the shot to the centre," said Honda.
"If it was saved, there was nothing I could do about it."
Japan coach Alberto Zaccheroni, who joined Japan after the 2010 World Cup, said his attractive Blue Samurai side would "surprise the world" at next year's tournament in Brazil.
"I came to Japan to bring them to the World Cup -- that was my bottom line," said the Italian. "I feel relieved that I achieved it. We are going to improve further and surprise the world."
Holger Osieck's Australia meanwhile will be glad of the point away from home as they scrap with Jordan, Oman and Iraq for the second automatic qualifying spot. The third-placed team will go into a play-off.
Japan had the better of a highly entertaining first half which saw chances fly thick and fast and heroic saves at both ends of the pitch.
Yasuhito Endo's dipping free-kick curled past the upright early on, and the Gamba Osaka midfielder then fired over the bar after a slick move orchestrated by Honda and Manchester United's Shinji Kagawa.
The same trio combined for another neat exchange which drew a one-handed reaction stop from Australia's Fulham goalkeeper Mark Schwarzer to deny Kagawa from close range.
At the other end Brett Holman dragged a shot wide, New York Red Bulls forward Tim Cahill volleyed over and Japan's Eiji Kawashima had to come sharply off his line after Robbie Kruse was put through one-on-one.
Kagawa and Honda continued to torment the Socceroos after the break and they nearly broke the deadlock on 55 minutes when the Manchester United man's stabbed, defence-flummoxing cross was poked wide by his bleach-blond team-mate.
Kagawa, operating on the left, was denied by hard-working Australian defender Sasa Ognenovski and then bounced a shot off the angle between the right post and the crossbar.
Zaccheroni brought on defender Yuzo Kurihara as a stalemate beckoned. But shortly afterwards, Oar silenced the massed Japanese fans when his cross from the left spun over Kawashima and crept in on 82 minutes.
Japan were staring at a cruel defeat but as the clock ticked to full time, Honda's cross was parried by McKay's arm. The blond CSKA Moscow talisman stepped up to ram the penalty past Schwarzer, who dived to his left.
"I think we performed better. We deserved a win. But as usual, something unexpected happened. But my players had a strong feeling to fight back," said Zaccheroni.
Japan are now through to their fifth straight World Cup since making their debut in 1998, and with a high-quality side which will look to build on their run to the last 16 four years ago in South Africa.
Australia have two games left to make sure of reaching their third World Cup in a row. The Socceroos, now level on points with second-placed Jordan, host the desert kingdom next week followed by Iraq on June 18.
