Tabei conquered Everest in May 1975, aged 35, before climbing all of the world's seven highest peaks by 1992.
She was diagnosed with cancer of the abdomen four years ago, and died in hospital in the city of Saitama.
Her last ascent was of Mount Fuji in July, alongside high school students affected by the 2011 Japanese earthquake and tsunami.
Tabei was originally from Fukushima prefecture, that was badly affected by the disaster.
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In 2012, Tabei told the Japan Times she was proud of how her ascent was viewed.
"Back in 1970s Japan, it was still widely considered that men were the ones to work outside and women would stay at home.
"Even women who had jobs - they were asked just to serve tea. So it was unthinkable for them to be promoted in their workplaces."
Her ascent of Everest came 12 days after she was swept away in an avalanche on the mountain. She was dug out by a guide and continued the expedition.
The first woman to ascend Everest, Japanese climber Junko Tabei, has died aged 77, her family say.