"It's the first time we have exercised with two carriers", said a Japanese military spokesman.
The Sea of Japan separates Japan from the Korean peninsula.
The USS Ronald Reagan and USS Carl Vinson strike groups operated in formation alongside Japanese forces in waters near the Korean peninsula Thursday, marking the largest display yet of naval power in response to North Korea's recent ballistic missile tests.
Meanwhile, Japanese Air Self-Defense Force F-15s are taking part in simulated combat with US Navy F-18 fighters at the same time, according to the Japanese military.
Japan's naval and air forces have launched a three-day joint military drill with U.S. aircraft carriers in the Sea of Japan amid tensions with North Korea over its missile and nuclear programs.
Although the Pentagon maintains that the aircraft carriers went there for routine deployments, and are not responding to any provocation in the region, the ballistic missile defense ships in the carrier strike groups represent an ideal match for any North Korean missile tests.
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Pyongyang's Korean Asia-Pacific Peace Committee said in a statement on Friday the United States "does not see reality properly, and if it continues to pursue military confrontation without success, we will hand them a big "bag of gifts".
North Korea which considers the deployments as an act of provocation, has threatened the U.S. with a nuclear attack in case of a direct military action.
The joint training comes after North Korea successfully carried out three ballistic missile tests in a month.
In a post on its Facebook page, the U.S. 7th Fleet described the drills as "routine training".
On Thursday, the U.S. Treasury Department imposed more sanctions on North Korea's military, coal companies and financial firms. It appears Japan and the United States are aiming to stop North Korea's reckless behavior by cranking up military pressure on Pyongyang.
"The U.S. special forces unit involved in such a raid would suffer significant losses", a Japanese government source said.