The jets have a top speed 1.6 times the speed of sound at almost 2000 km/h.
Flanked by the ageing F-18 Hornets they're set to replace, the first two F-35s landed at RAAF Base Williamtown on Monday after flying from RAAF Amberley in south Queensland, where they arrived from the United States last week.
Aviation enthusiasts gathered on the edge of the base from early in the morning and more watched a flyover of Newcastle ahead of the state-of-the-art aircraft's official welcome by Defence Minister Christopher Pyne.
The delivery has been 16 years in the making under the US-led Joint Strike Fighter program aiming to develop a global fleet of 1000 advanced jets.
Australia will spend an estimated $17 billion on 72 of the F-35 aircraft. The cost has been widely criticised including by US President Donald Trump.
The exact cost of maintaining the aircraft won't be known until the end of 2020.
By that time, Australia is expected to have an operational fleet of 12, and another 18 fighters on the ground.
Williamtown and RAAF Base Tindal in the Northern Territory will eventually host four squadrons with a fifth an option should the order increase to 100 jets.
Lockheed Martin, builders of the jets, say the cost is expected to be driven down to $80 million per plane by 2020.
Former prime minister Malcolm Turnbull backed the spending when questioned in 2017.
"When we send our young men and women out to war, they have the tools to do the job to destroy their enemies and the terrorists," he said.
The national audit office's report into the project found Defence had established effective transition planning and project governance.
But the report said it failed to provide annual updates to government and once committed $266 million to a section of the project without first consulting the prime minister or finance minister as required.