After the break, Japan pressed a exhausted Colombia side and Yuya Osako grabbed the victor with a glancing header in the 73rd minute.
In an explosive start to the Group H clash, Colombia defender Carlos Sanchez earned the first red card of Russian Federation 2018 with a handball after just four minutes. This scoreline was particularly unexpected in light of the fact that Japan had changed coaches shortly before the tournament, and because no Asian team had ever previously defeated a South American side in 17 World Cup meetings.
Indeed, the nation were without James Rodriguez, the midfielder who lit up the 2014 tournament in Brazil, from the start due to injury, though he did come off the bench in the second half.
So Sanchez's right arm movement sent Japan to the spot.
Colombia and Japan open World Cup Group H play against each other when they face off in Saransk, Russia.More news: Children Separated From Parents At Us Border Sob, Wail Desperately
But Colombia, having wrestled a foothold in the game, rarely threatened in the second half as Japan took control.
James Rodriguez was left out of Colombia's starting line-up for their opening World Cup match against Japan on Tuesday as the Brazil 2014 top scorer labours with a calf strain.
Japan became the latest side to pull off an upset at the World Cup, joining Mexico, Switzerland and Iceland in earning surprising results. The South Americans are the better team, and are very much capable of stealing a point or three.
Group H kicked off today as the first round of games at the World Cup comes to an end.
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Victory over Colombia will give Japan hope of progressing beyond the group stage for the first time since 2010, while Pekerman will hope that James can return to full fitness in time for their forthcoming clash with Poland.