Ryoko Azuma, 44, will command four warships making up a division with a total of 1,000 crew members.
"This is the first time a woman was appointed for the job," a spokesman for the Maritime Self-Defence Force told AFP.
"But she wasn't chosen because she was a woman."
The ships include the helicopter carrier Izumo, the navy's biggest ship.
"I want to do my best to carry out the heavy duty I have been given," Azuma told reporters after a ceremony at Yokohama near Tokyo to mark her arrival in the post.
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"I don't think about being a woman but I want to try to become a role model for younger female officers," she said.
About 14,000 women are currently serving in the Self-Defence Forces as the military is known, accounting for only six per cent of the entire personnel.
On most levels, Japan lags behind other developed countries in terms of sexual equality.
In politics women are still under-represented with only 47 of the 465 members of the lower house.
According to statistics compiled by the Swiss-based Inter-Parliamentary Union, this ratio of 10.1 percent places Japan below Myanmar and Gambia.