Not overawed by the big occasion, Amajita started the game on the front foot, their crisp passing and ball retention starving the Japanese of possession in the early stages.
And just seven minutes in, Thabo Senong’s men were in front as Grant Margeman beat the offside trap and sent a ferocious strike goalwards which deflected off Japanese defender Takehiro Tomiyasu to give the South Africans the early advantage.
With their tails up, Amajita had numerous chances to double their lead soon after, Luther Singh blasting his effort wide before Keletso Makgalwa missed a golden chance, heading wide with just the goalkeeper to beat.
Japan then started to settle and see more of the ball, creating the better chances with Koki Ogawa their danger man: the number nine watched his effort from a corner bounce back off the cross bar before trying his luck from range with no end product.
Ogawa was left unmarked moments later but could only head wide, before teammate Kou Itakura also missed the target with his headed chance.
Amajita spurned a glorious opportunity with ten minutes left in the half as a brilliant run down the right by Makgalwa saw the lively attacker find Singh, who twisted and turned in the box before unleashing a ferocious effort off target.
The Asians ended the half the stronger of the two sides, with Koji Miyoshi coming closest after a poor clearance by the South Africans, yet his effort at an empty goal curled wide.
Japan began the second stanza as they finished the first, and were rewarded as Ogawa finally got his goal, squeezing the ball past Mpoto and over the line.
The Asian side kept pressing and asking questions, with Mpoto equal to the task each time, denying Ogawa in a one-on-one situation after 15-year-old substitute Takefusa Kubo thread the striker through on goal.
Singh’s effort was then blocked at the other end of the pitch in a rare attack for the South Africans, who eventually succumbed to the Japanese pressure as impressive combination play by Kudo and Ritsu Doan resulted in the latter slotting home to give his side the lead on 72 minutes.
Mpoto was the busier of the two keepers in the closing stages as Amajita failed to unlock a stubborn Japanese defence, with the Asian giants emerging 2-1 victors in an entertaining group stage match-up.
South Africa will look to pick themselves up as they prepare for a clash against Italy on Wednesday, while Japan take on Uruguay.
Meanwhile, Amajita's African rivals Guinea started off their tournament with a 3-0 loss to Korea Republic while Zambia marked their return to the competition after 10 years with a 2-1 victory over Portugal.
South Africa U-20 XI: Mpoto; Mukumela; Modise; Malepe (C); Mthethwa; Meyiwa (Jordan 75’); Cele; Mbatha; Singh; Margeman; Makgalwa (Kodisang 65).