The deployment of the 10 planes to Marine Corps Air Station Iwakuni on Honshu Island marks a major milestone for the F-35, which has been bedeviled by technical glitches and soaring cost overruns.
With a current development and acquisition price tag already at $379 billion for a total of 2,443 F-35 aircraft, Lockheed Martin's F-35 is the most expensive plane in history, and costs are set to go higher still.
The Marines's version of the plane, known as the F-35B, is capable of conducting short takeoffs and vertical landings.
Trump last month sent shockwaves through the aerospace industry when he tweeted that he wanted rival Boeing to price out a possible alternative.
"Based on the tremendous cost and cost overruns of the Lockheed Martin F-35, I have asked Boeing to price-out a comparable F-18 Super Hornet!" Trump tweeted December 22.
The F/A-18 Super Hornet does not have stealth capabilities and has been in use since the late 1990s.
Once servicing, maintenance and other costs for the F-35 are factored in over the aircraft's lifespan through 2070, overall program costs have been projected to rise to as much as $1.5 trillion.
Proponents of the F-35 tout its speed, close air-support capabilities, airborne agility and a massive array of sensors giving pilots unparalleled access to information.
"The unique combination of stealth, cutting-edge radar and sensor technology, and electronic warfare systems bring all of the access and lethality capabilities of a fifth-generation fighter, a modern bomber, and an adverse-weather, all-threat environment air-support platform," the Marines said in a statement.
In August, the US Air Force declared an initial squadron of F-35A stealth fighters ready for combat and said an overseas deployment for that version of the plane was likely early this year.
The US Navy's version of the plane, the F-35C, is built to land on aircraft carriers.