Former prime minister Mori, 83, quipped during a meeting of the Japanese Olympic Committee that women talked too much.
The Olympics overlord initially defied calls to quit over his sexist jibes. But a petition drive led by a 22-year-old rights activist as well as questions about his continued suitability from leading sponsors forced his hand.
Hashimoto announced her selection shortly after submitting her resignation as Olympics minister to Prime Minister Yoshihide Suga,
"As I’m taking on such a grave responsibility ... I feel I need to brace myself,” Hashimoto said.
Progress
Her appointment was welcomed by the Japanese tennis star Naomi Osaka who condemned Mori's comments as ignorant.
"I feel like it's really good because you're pushing forward, barriers are being broken down, especially for females," said the 23-year-old after beating Serena Williams on Thursday to reach the Australian Open final.
"We've had to fight for so many things just to be equal. Even a lot of things, we still aren't equal."
Hashimoto, 56, competed in four winter games as a speed skater and three summer events as a cyclist. Her only medal - a bronze - came in the 1992 games in Albertville.
Qualifications
Criteria for a new leader for the organising committee included a deep understanding of gender equality and diversity. Hashimoto, who had been the Olympics minister since 2019, doubled also as minister for women's empowerment.
Not only will she have to clear up Mori’s antediluvian antics, she will also have to woo sceptics. Several polls have shown increasing domestic opposition to the games amid the coronavirus pandemic.
Foreign Olympic committees will also be seeking assurances about health protocols before agreeing to send their athletes to Tokyo for the event.
The 32nd Olympiad was scheduled for the summer of 2020 but it was eventually postponed as the first wave of the coronavirus pandemic took hold.
It was thought the disease would be under control a year later. But variant strains have continued to increase the death toll even though vaccination programmes have been launched around the world.
The Games are scheduled to begin on 23 July and will last until 8 August.