Osaka Mayor Toru Hashimoto said on Monday that the "comfort women" gave Japanese soldiers a chance "to rest".
On Tuesday, Japanese ministers tried to distance themselves from his remarks.
Some 200,000 women in territories occupied by Japan during WWII are estimated to have been forced to become sex slaves for troops.
Many of the women came from China and South Korea, but also from the Philippines, Indonesia and Taiwan.
Japan's treatment of its wartime role has been a frequent source of tension with its neighbours, and South Korea expressed "deep disappointment" at Mr Hashimoto's words.
"There is a worldwide recognition... that the issue of comfort women amounts to a war-time rape committed by Japan during its past imperial period in a serious breach of human rights," a South Korean foreign ministry spokesman told news agency AFP.
Mr Hashimoto is the co-founder of the nationalist Japanese Restoration Party, which has a small presence in parliament and is not part of the government.
He was the youngest governor in Japanese history before becoming mayor of Osaka, and last year said Japan needed "a dictatorship".
In his latest comments, quoted by Japanese media, he said: "In the circumstances in which bullets are flying like rain and wind, the soldiers are running around at the risk of losing their lives,"
"If you want them to have a rest in such a situation, a comfort women system is necessary. Anyone can understand that."
He acknowledged that the women had been acting "against their will". He also claimed that Japan was not the only country to use the system, though it was responsible for its actions.
He said he backed a 1995 statement by Japan's then-PM Tomiichi Murayama, in which he apologised for war-time actions in Asia.
"It is a result of the tragedy of the war that they became comfort women against their will. The responsibility for the war also lies with Japan. We have to politely offer kind words to [former] comfort women."
On Tuesday Japan's Cabinet Minister Yoshihide Suga declined to comment directly on Mr Hashimoto's remarks but reiterated the government's existing stance on comfort women.
He said the government felt "pains towards people who experienced hardships that are beyond description".
In 1993, Japan issued an apology for the "immeasurable pain and suffering" inflicted on comfort women. In 1995, it also apologised for its war-time aggression.
Education Minister Hakubun Shimomura also expressed concerns over Mr Hashimoto's remarks.
"A series of remarks related to our interpretation of (wartime) history have been already misunderstood," he told reporters. "In that sense, Mr Hashimoto's remark came at a bad time."
Last month, Japanese Prime Minister Shinzo Abe angered China and South Korea when he suggested he may no longer stand by the wording of Japan's 1995 apology, saying the definition of "aggression" was hard to establish.
Japanese ministers later sought to play down his remarks, amid anger across the region.
Japan's neighbours also objected to visits in April by several cabinet members and 170 MPs to Japan's Yasukuni shrine, which honours Japan's war dead, including war criminals.
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