Nacer Chadli scored the victor in the fourth minute of added time, finishing a breakaway move to leave Japan's players in tears at the final whistle.
Belgium are going through to face Brazil in the quarter-finals. And despite dominating possession, Belgium failed to create many other quality chances while Japan looked unsafe throughout the first half on the counter-attack.
Fox Sports timed the counterattack at 9.9 seconds.
After a goalless first half, Japan struck twice in seven minutes following the interval to take full control of a gripping last-16 tie in Rostov-on-Don on Tuesday morning (AEST).
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The official had to check with the Video Assistant Referee (VAR) before confirming the goal, but it was good. It is the fourth time in five World Cups that the holder has failed to make it out of the group stage.
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Belgium very almost responded instantly, with Eden Hazard rocketing a shot off the post just after the reset.
Japan started off their World Cup campaign with a victory over 10-man Colombia as Shinji Kagawa and Inui scored for the Japs to win 2-1 over Colombia.
Unfortunately for Japan, the lead would prove short-lived.
Substitute Fellaini astonishingly drew Belgium level to huge sighs of relief after heading home an excellent Eden Hazard cross to make the scores 2-2.
The Red Devils were still struggling but they pulled a goal back after 69 minutes when Vertonghen looped a header from a high clearance back across goal into the far top corner.