Faced with growing Chinese military clout and a nuclear-armed North Korea, the Japanese government plans to double its defence spending to the NATO standard of two percent of GDP by 2027.
A sale of up to $2.35 billion for two types of Tomahawks, which have a 1,600-kilometre (995-mile) range, was approved by Washington in November.
"The conclusion of this signing starts the procurement of the Tomahawk missiles," a defence official told reporters on Thursday after the deal was signed in Tokyo.
"Through sound implementation of the (defence) budget, we will extensively strengthen our defence capacity," he added.
Japan has approved a record defence budget worth $56 billion for the next fiscal year from April.
Japan has a pacifist post-war constitution, which limits its military to ostensibly defensive measures.
But when it updated key security and defence policies last year, Tokyo explicitly outlined the challenge posed by China.
At a press conference earlier in the day, US ambassador Rahm Emanuel lauded Japan's new defence push.
"As aggressors grow more and more belligerent, Japan is at the forefront of countries rallying to protect peace and prosperity by raising the costs of aggression," he said.
Last month Tokyo loosened arms export controls to enable it to sell Patriot missiles made in Japan under licence to the United States, which is seeking to replenish its stocks after sending the weapon systems to Ukraine.
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