Striker Atsushi Yanagisawa put the Asian champions in front in the 63rd minute and substitute Masashi Oguro added a second a minute from time to secure Japan's third World Cup appearance.
North Korea striker Kim Yong-su was sent off in stoppage time for stamping on Makoto Tanaka, who was lucky to escape a red card himself for lashing out at his opponent.
"We've had lots of criticism but the team have done the job we came to do," Japan coach Zico told reporters. "We have shown tremendous resilience, guts and mental strength. We deserve to be through."
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FIFA moved the politically charged clash to Bangkok as punishment for crowd violence following North Korea's 2-0 defeat by Iran in Pyongyang in March.
Japan qualified for their first World Cup finals in 1998 and co-hosted the 2002 tournament with South Korea.
Italy-based midfielders Hidetoshi Nakata and Shunsuke Nakamura were both suspended for the Group B game but Japan, who only needed a point, always looked in control.
Yanagisawa slid in to volley home from close range after 73 minutes to settle Japan's nerves. Oguro latched on to a pass from Tanaka to add a late second.
The final whistle was greeted by wild celebrations from the Japanese players and coaching staff that echoed around the empty stadium.
North Korea's outside chance of reaching the World Cup for the first time since 1966 ended with their fifth straight defeat.
Japan provisionally climbed above Iran at the top of Group B with 12 points from five matches.
Iran have 10 points and can secure a World Cup place for the third time with a point at home to Bahrain later on Wednesday.
Saudi Arabia and South Korea also hope to qualify with victories in Group A.
The top two teams from each group advance automatically. A fifth Asian team could qualify for next year's World Cup finals via a playoff with a CONCACAF team.
The two third-placed teams in each Asian group face each other over two legs and the winners play the fourth-placed team in the North, Central America and Caribbean region.
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