The move could further inflame already-strained ties in the region, where clashes over differing interpretations of history frequently mar important economic relationships.
Revised teachers' manuals for junior and senior high schools will be issued to education boards across the nation, an education ministry official said.
"From the educational point of view, it is natural for a state to teach its children about integral parts of its own territory," Education Minister Hakubun Shimomura told a news conference.
The move comes as Prime Minister Shinzo Abe has stirred controversy with his unabashed nationalism, including with a visit to a war shrine widely viewed by neighbouring countries as a symbol of Tokyo's wartime aggression.
Japan is embroiled in a row with China over the Tokyo-controlled Senkaku islands in the East China Sea, claimed as the Diaoyus by Beijing.
The dispute regularly sees standoffs between paramilitary ships and has also involved military vessels and planes. Some observers say the islands represent a key fault line for the region and could be the spark for an armed conflict.
Tokyo and Seoul, meanwhile, are at odds over the sovereignty of a pair of sparsely-inhabited rocks in waters between them, administered by Seoul as Dokdo, but claimed as Takeshima in Japan.
The new manuals describe both sets of islands as "integral parts of Japanese territory" for the first time, the official said.
The manuals will also note that the Takeshima islands are "illegally" occupied by South Korea, and that Japan does not even recognize the existence of a territorial dispute over the Senkaku islands, the official said.
The current manuals instruct teachers only to refer to a difference in Japanese and South Korean positions on Takeshima, while there were no remarks on the Senkakus.