Japan's defence establishment was taken aback by the US President Donald Trump's recent decision to halt "expensive" military exercises with South Korea that have always been seen in Tokyo as a deterrent to North Korea's threats.
There are also concerns in Tokyo and Seoul that Washington could reach a deal with North Korea that would remove the threat of Pyongyang's long-range missiles that can reach America but leave Japan and South Korea at the mercy of shorter-range weapons.
Mattis stressed that Washington's alliance with Japan was a "cornerstone" of regional stability, as he wrapped up a four-day Asian visit in Tokyo following talks with his counterpart Itsunori Onodera aimed at reassuring partners in the region.
The U.S. defense secretary also explained to his counterpart about the issues discussed at Wednesday's meeting with Chinese President Xi Jinping and the results of the talks.
"We look to cooperate where and when possible and we will compete vigorously where we must", he said.
"At the same time, we maintain a strong collaborative defensive stance to ensure our diplomats continue to negotiate from a position of unquestioned strength", he added.
He assured the South Korean government of an "ironclad" commitment to its security, including keeping USA troop levels there of around 28,500 soldiers.
Washington's decision to halt the exercises after an unprecedented summit between US President Donald Trump and North Korean leader Kim Jong Un surprised officials and observers in the region.
Both South Korea and Japan have security alliances with the United States guaranteed by treaty, but have been thrown off-balance by Trump's quick moves on negotiations with Kim.
In Singapore, Kim signed a document committing the North to "work toward complete denuclearization of the Korean Peninsula"-a vague term open to interpretation on both sides, and critics said the declaration lacked substance and specifics".
Following the defense chiefs' meeting, Mattis went on to meet Japanese Prime Minister Shinzo Abe and the pair spoke of the importance of maintaining the two nations' bilateral alliance.
"If North Korea maintains its commitment to denuclearization and proves its willingness with actions, we will continue to devise measures to build mutual trust and establish peace", he said.
North Korea, which has previously vowed to sink the Japan into the sea, fired two test missiles over the island nation a year ago, with others splashing into the sea nearby.
Responding to another key concern of Japan, Mattis highlighted following talks with Defense Minister Itsunori Onodera the plight of Japanese nationals allegedly abducted by North Korea.
Underscoring the point, he presented a blue tie with a Pentagon motif to Onodera, telling him "to remember you have a friend in the Pentagon".
Aircraft safety has been an increasing issue.
"We shared our understanding of the situation in the East and South China seas and once again we affirmed that Article 5 of the Japan-U.S. security treaty applies to the Senkaku Islands", Onodera said. "There are a lot of things that still need to be worked on there".