Ayase Ueda grabbed the winning goal on Tuesday with a header in the 71st minute, sending the sell-out crowd into wild celebrations.
It was Japan's first win over the South American giants, at the 14th attempt.
Brazil coach Carlo Ancelotti made several changes to the team that won 5-0 in South Korea four days ago, but the five-time world champions continued their strong form from Seoul with a dominant first half in the Japanese capital.
Goals from Paulo Henrique and Gabriel Martinelli put the visitors seemingly in control at halftime, and a 12th win over Japan appeared likely.
Seven minutes after the restart, however, Takumi Minamino capitalised on a mistake by Cruzeiro defender Fabricio Bruno to score from inside the area. Just after the hour, Keito Nakamura's shot deflected off Bruno to bring Japan level.
Ancelotti, who took charge in May following Brazil's inconsistent World Cup qualifying campaign, urged his players to develop greater mental resilience.
"No, everything is not fine," Ancelotti told a press conference. "When the team loses, we are upset, which is normal. Everyone is upset. I don't like to lose, and neither do the players. We have to learn from this defeat, as we always do in football.
"Until Bruno's mistake on the first goal, the game was well controlled. After that, the team fell apart mentally."
Both teams have already qualified for the 2026 World Cup which will be co-hosted by the United States, Canada and Mexico.
With Reuters
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