Keisuke Honda enjoyed a belated birthday celebration as Japan regained that winning mentality.
The CSKA Moscow attacker, 24 yesterday, got the all-important goal after 39 minutes of the Group E match at the Free State Stadium.
It meant a long-awaited victory for coach Takeshi Okada, who had seen his side lose four and draw one of their warm-up matches, scoring only one goal in the process.
He had claimed before the game, however, he was not worried about Japan's poor form going into the competition.
While Okada opted for a lone striker in Yoshito Okubo, his Cameroon counterpart Paul Le Guen decided on an adventurous 4-3-3 formation.
Despite being one of Africa's brightest hopes Cameroon were toothless, despite having a great deal of possession, although goalkeeper Eiji Kawashima made a breathtaking save from substitute Mohamadou Idrissou in stoppage time.
Much was expected of skipper Samuel Eto'o but the Inter Milan striker was left frustrated as Japan defended in numbers.
Le Guen saw his side carve out the first opening of the game in the eighth minute when Eto'o released Pierre Webo.
He raced to the byline and played the ball into the middle but Eyong Enoh was unable to get a decent touch.
Kawashima then made a good block from Enoh's close range effort before Japan made the breakthrough.
The Cameroon defence failed to cut out Daisuke Matsui's cross to the back post and Honda reacted quickly. He got a superb first touch before clipping the ball beyond a stranded Souleymanou Hamidou.
It was just what Japan wanted and they had also kept Eto'o quiet in the first half.
Cameroon came out with a purpose at the start of the second half and should have equalised in the 49th minute.
Eto'o got the better of two players in a determined run. He played the ball into the path of Eric Choupo-Moting who was clear in front of goal.
However the striker failed to test Kawashima, his effort going wide of the post to Japan's relief.
Cameroon were enjoying a decent spell and Choupo-Moting cut inside only to drag his shot off target.
However Japan almost added a second goal in the 82nd minute when they launched a swift counter-attack.
Makoto Hasebe's shot was parried by the goalkeeper but only landed at the feet of substitute Shinji Ozakaki, who saw the rebound come off the outside of the left post.
Cameroon responded and three minutes later Stephane Mbia's instinctive effort rattled the bar.
With the crowd urging them, Cameroon kept pushing players forward in search of the equaliser but Japan stood firm.
However they had to rely on Kawashima right at the end to give them the victory they had craved.
The Kawasaki Frontale shot-stopper has only recently taken the jersey and it was easy to understand why as Cameroon were left frustrated.
Former Lyon, Rangers and Paris St Germain boss Le Guen was hoping Cameroon would make it through to the quarter-finals, but this opening defeat makes that looks an outside bet at the moment, with group rivals Holland also chalking up a victory earlier in the day.