Saudi Arabia wants American F-35s. Israel’s success with them shows why.

Former senior Israeli defense officials say a major reason for that success—and for Israel’s ability to dominate battlefields from its own backyard to more than 1,000 miles away—is the F-35. Now, with the Trump administration agreeing to sell the most expensive and advanced U.S. aircraft to Saudi Arabia, there is concern in Israel that it could lose a pillar of its uncontested military advantage over its neighbors.

This issue for Israel isn’t with the current government of Saudi Arabia. Instead, Israel fears that sales to the kingdom could open the door to others in the region, like Turkey, that have their own aspirations for the warplane. Such a sale would erode Israel’s advantage and put its own F-35s at greater risk at a time when the regional balance of power is shaped largely from the air.

“The long borders and multiple fronts make it difficult to have enough ground fire," said Eyal Hulata, former head of Israel’s National Security Council and now a fellow at the Foundation for Defense of Democracies. “Our air force is our insurance policy. It is our long arm but also our quickest and most effective response to most situations."

Technology leaders like Elon Musk and others have criticized the F-35 for its high cost of about $100 million per plane, its complexity and downtime, but Israel has been an early and frequent user of the jet, and has put it in heavy rotation in arenas from Lebanon to Yemen to Iran.

The jets are extremely stealthy and can carry large payloads further than 1,300 miles. Equally important are the onboard sensors and radar that give pilots an extensive view of the battlefield, as well as networking capabilities that let pilots integrate with each other and even control squadrons of accompanying drones.

Israel used the F-35s to great effect in its 12-day war against Iran in June. The stealth-fighters’ capabilities and advanced radar and targeting systems allowed Israel to batter Iran’s air defenses at the start of the war, giving it air superiority in Iranian skies.

“When you look at the whole operation, with no human casualties, with only some unmanned platforms lost, it’s a huge achievement," said Assaf Orion, a Washington Institute research fellow who served as the head of strategy for the Israel Defense Forces from 2010 to 2015. “It shows you the level of air force that can be built around the F-35."

One fear among Israelis is that if the Saudis get F-35s, they will have the ability to spot Israeli F-35s, said Yaakov Amidror, a former Israeli national security adviser and now a fellow at the Washington-based Jewish Institute for National Security of America.

“The fact that Israel was the only country with F-35s in the region was very important," Amidror said. “It gave us opportunities that allowed us to make operations without being exposed by others, and it gave us an advantage in defensive operations."

Israel has also improved upon the F-35s, adding their own upgrades and capabilities and learning lessons from its combat use that it has shared with the U.S. Amidror says the country would want a say in whether such enhancements are shared with other buyers in the region.

Arab governments were stunned by the reach and precision of Israel’s military operations over the past two years and have grown concerned about the lopsided balance, specifically calling out their lack of F-35s.

Israel’s intelligence services have also contributed significantly to the country’s military superiority. It supplied extensive real-time target lists in Tehran and supplied the Lebanese militia Hezbollah with doctored pagers that it then remotely detonated.

But Israel’s security establishment is worried that its advantage could be eroded in light of force buildups in countries like Egypt and Turkey.

“Israel is struggling to maintain its qualitative military edge also because we are in a growing quantitative disadvantage," Hulata said. “The force buildup in countries like Egypt and Turkey is tremendous, and while we have peace with both at the moment, there is also growing tension, and Israel must prepare for contingencies."

Israelis are concerned that while Riyadh isn’t currently a foe, that may not always be the case. The two countries are just minutes apart if Saudi jets are based near the Israeli city of Eilat, a port town on the Red Sea.

Orion points out that Iran still has U.S. F-14s. “Weapons systems outlive regimes," he said.

Despite the concerns, former senior Israeli and American officials said Israel will maintain its military superiority as long as the two countries agree on new levels of cooperation and the acquisition of new technologies to offset whatever edge has been lost.

It also could take a long time for Saudi Arabia to actually take possession of the jets and the process could get gummed up in Congress or derailed by other developments. Trump agreed in 2020 to sell F-35s to the United Arab Emirates, but the deal ultimately fell apart.

Daniel Shapiro said he was familiar with the talks between Washington and the U.A.E. over the plane when he served as deputy assistant secretary of defense for the Middle East in the Biden administration. He said Israel and the U.S. had worked out how to maintain Israel’s qualitative military edge.

“There are all kinds of details about the capabilities, its basing, terms of use, and then of course what Israeli capabilities are that can counter any kind of threat that can bear on the question," Shapiro said, who also served as U.S. ambassador to Israel in the Obama administration.

He noted the sale of F-35s will have to be approved by Congress, which will hear Israel’s concerns, and that the U.S. government is bound by law to preserve Israel’s military advantage in the region.

The U.S. and Israel could also try to use the sale to encourage Saudi Arabia to normalize relations with Israel. That would lower the possibility of a clash and fundamentally change the geopolitical risks in the region.

“What changes the power of balance in the Middle East is normalization between Israel and Saudi Arabia," Hulata said. “To get that there are various things Israel should be expected to provide. One is approval of advanced weaponry."

Write to Dov Lieber at dov.lieber@wsj.com