The Japanese Self Defence Forces' destructor vessel Izumo, which allows for the simultaneous take-off and landing of five helicopters, set sail towards the Pacific from the Yokosuka navy base, south of Tokyo, Efe news reported.
The 19,500-tonne ship will escort a US supplies vessel towards the island of Shikoku, before beginning a three-month voyage, in what will be its first such mission in over 70 years.
Izumo will support the US vessel, responsible for providing fuel and other supplies to American vessels in the region, including the nuclear-powered aircraft carrier USS Carl Vinson and its attack fleet.
Washington dispatched this fleet to waters off the Korean Peninsula in response to repeated missile tests by Pyongyang, and amid fears that the regime may be preparing to carry out its sixth nuclear test.
Pyongyang conducted its latest missile test on Saturday, the same day that the US carrier reached the Sea of Japan and conducted military drills with Japanese and South Korean troops.
The dispatch of Izumo is the first mission by Japan to back allied troops since 1945, when World War II came to an end.
The expedition follows the reinterpretation of Article 9 of the Japanese Constitution, with the government led by Prime Minister Shinzo Abe recognising collective self-defence and expanding the powers of its troops to defend and provide logistical support to allies.
The country's security forces were previously only permitted to use force in self-defence.