The State Department said it was approving the $2.35 billion sale that includes two types of the Tomahawk missiles, which have a 1,600-kilometer (995-mile) range.
The State Department said the sale was aimed at "improving the security of a major ally that is a force for political stability and economic progress in the Indo-Pacific region."
The sale "will improve Japan's capability to meet current and future threats by providing a long-range, conventional surface-to-surface missile with significant standoff range that can neutralize growing threats," it said in a statement.
Prime Minister Fumio Kishida told a parliamentary committee in February that his government was seeking 400 Tomahawk missiles as part of a major defense push.
Japan has been alarmed by China's growing military clout, including its exercises around Taiwan, as well as by nuclear-armed North Korea's missile tests.
The missile deal is going ahead despite dialogue with China aimed at easing tensions.
Chinese President Xi Jinping met separately in recent days on the sidelines of an Asia-Pacific summit in San Francisco with Kishida and US President Joe Biden.
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