Makeshift striker Keisuke Honda's 39th minute goal ended a dismal five-match winless run with just one goal scored while Cameroon's Indomitable Lions proved toothless and skipper Samuel Eto'o had a largely ineffective game.
Indeed, the Japanese fans who wore blue T-shirts with the slogan "Eto'o Who?" were proved right.
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Japan join the Netherlands as the day's Group E winners after the Dutch beat Denmark 2-0 in the early match.
Man of the match Honda, who celebrated his 24th birthday on the eve of the game, told reporters: "Recently our team has not been delivering very good results and to be honest the mood was not the best but with our coach as the focus of our team we have delivered our best and this very good result today."
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Japan cocach Takeshi Okada, who just last month offered his resignation following a friendly defeat to South Korea, barely savoured the victory, saying he was already looking ahead.
"The next game we will be up against the Netherlands so we have to go further. This is the first win for us on foreign soil, but this is not an achievement for us at all, what is coming next is the point.
"Today our players have done a good job but what we have to do against the Netherlands was the immediate thought that I had after the game."
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Le Guen had talked of matching the Lions' 1990 achievement, when they beat holders Argentina and reached the quarterfinals and must now aim to overcome Denmark in Pretoria on June 19 to keep hopes of achieving that goal alive.
"We have to win against Denmark, we know that, we will try to recover well to do our best," a downbeat Cameroon coach Paul Le Guen told reporters.
Le Guen had omitted experienced midfielder Alexandre Song from the starting line-up, giving Joel Matip the nod in a three-man midfield which failed on too many occasions to feed the ball to their front three.
Pushed on by their drum-beating fans, Cameroon improved after the break. Eto'o scared Japan when he beat four players down the right wing before setting up Eric Choupo Moting, who curled his shot wide of the far post.
Stephane Mbia hit the bar late on with a rasping 30 metre drive but the African side did not threaten enough as Japan left Honda up front while the rest defended their lead.
Japan's only two previous victories in the finals came in 2002 as joint hosts of the tournament with South Korea.
For Cameroon, the resul
