The deal, approved by Israel's Ministerial Committee on Procurement, is a first step in a 350 billion shekel ($A165 billion) plan to bolster Israel's military and "strengthen readiness ahead of a demanding decade for Israeli security", the ministry said on Sunday.
It said the new squadrons would serve as a cornerstone of the military's long-term force development, addressing regional threats and preserving Israel's strategic air superiority.
"Alongside immediate wartime procurement needs, we have a responsibility to act now to secure the IDF's military edge 10 years from now and beyond," ministry director general Amir Baram said, referring to the Israel Defense Forces.
The recent war with Iran "reinforced just how critical the US-Israel strategic relationship is, and how essential advanced air power remains", he said.
Under the deal, Israel would buy a fourth F-35 squadron from Lockheed Martin and a second squadron of F-15IA fighter jets from Boeing.
In December, Boeing was given an $US8.6 billion ($A11.9 billion) contract for Israel, including 25 new F-15IAs and an option for 25 more.
Baram said the next step would be to move forward with finalising the agreements with the US government and military counterparts.
The US and Israel launched air strikes on Iran on February 28, but a ceasefire has been in place since April 8.
The US Navy maintains a blockade of Iranian ports.
Defence Minister Israel Katz said the Iranian conflict demonstrated the air force's power and its decisive role in protecting Israel.
"The lessons of that campaign require us to keep pressing forward on force build-up, to ensure air superiority for decades to come," he said.
Israeli aircraft have also attacked Iranian-backed Hamas militants in Gaza and Hezbollah militants in Lebanon since the October 7, 2023, Hamas attacks on Israel.
Katz said the new aircraft would lead to a significant technological leap in integrating autonomous flight capabilities, next-generation defence systems, and establishing Israeli military dominance in space.
"Our mission is clear: to ensure the IDF has the tools, capabilities, and strength to operate anywhere, at any time," Katz said.
"We will continue to invest, to grow stronger, and to stay ahead of our enemies - to keep Israel secure today and in the future."