It was also a belated birthday present for Honda, who had turned 24 the day before.
The Blue Samurai, struggling for goals in the run-up to the tournament, took the lead in the 39th minute and held on for the remainder of the match despite increasing pressure from the African side in the second half.
Neither side looked capable of breaking the deadlock in a scrappy first half in which clear chances were in short supply until Daisuke Matsui maneuvered the ball onto his left foot and delivered an inswinging cross from the right.
The ball somehow eluded several Cameroon defenders, and the unmarked Honda stabbed it past the despairing dive of Hamidou Souleymanou to give Japan the lead.
Four minutes after the re-start Cameroon went close to an equalizer when Eric Choupo Moting fired wide following good work on the right by Inter Milan star Samuel Eto’o.
It was the first significant contribution from three-time African Player of the Year Eto’o, who struggled to make an impact on the game after being deployed in a deep-lying role.
Despite a more open game in the second half, the goalkeepers remained relatively untroubled in the early stages.
As Cameroon continued to press for an equalizer, they threw on Achille Emana, Mohamadou Idrissou and veteran Geremi, but could still not find a way past the dogged Japanese defense.
Japan came close to doubling their lead as time ran out, with substitute Shinji Okazaki, on for Matsui, hitting the post after a fierce shot by captain Makoto Hasebe was parried by Souleymanou.
With just five minutes remaining Stephane Mbia let fly with a thunderbolt from 25 yards that rattled the Japan crossbar but they could not find a way past Japan goalkeeper Eiji Kawashima.
Pierre Webo got his foot on a cross as the clocked ticked down but Kawashima made a fine scrambling save.
Earlier, in cool conditions at the high-altitude Free State stadium the crowd whipped up a lively atmosphere despite banks of empty white seats but neither side could settle into a rhythm.
Japan’s goal came moments after Cameroon hit the first shot of the game on target, with Eyong Enoh hitting the ball straight at Kawashima.
Japan next face group favorites the Netherlands on Saturday after the Dutch beat Denmark 2-0 in Johannesburg to take an early lead in Group E.
BLOEMFONTEIN, SOUTH AFRICA – JUNE 14: Eiji Kawashima (R) of Japan celebrates with Yuto Nagatomo (L) and Marcus Tulio Tanaka after the 2010 FIFA World Cup South Africa Group E match between Japan and Cameroon at the Free State Stadium on June 14, 2010 in Mangaung/Bloemfontein, South Africa. (Photo by Ian Walton/Getty Images) *** Local Caption *** Eiji Kawashima;Yuto Nagatomo;Marcus Tulio Tanak