One of his biggest challenges will be balancing the company's dependence on China while parrying acute political pressure from the White House.
The handover ends Tim Cook's 15-year run, replacing the operations specialist who built Apple's supply chain with the engineer who built its hardware.
Ternus, 51, joined Apple's design team in 2001 and worked his way up to senior vice-president of hardware engineering, reporting to Cook.
He leads the engineering teams behind Apple's entire product line-up, including the iPhones that generate most of the company's revenue.
He gets barely a week to settle in, with Apple holding its annual iPhone event on September 9, where it is expected to unveil its first foldable handset.
"Tim Cook left the house in phenomenal order," said Dan Ives, partner and senior managing director at investment firm Yorkville Ives & Co.
"But now it's about Ternus defining the AI chapter."
Ives expects the new chief executive to lean into what he knows.
"There's no reason to fix what's already working," he said, predicting Ternus will concentrate on hardware innovation while leaving Cook's supply chain intact.
Some analysts had argued software chief Craig Federighi was the more logical pick for a company scrambling to catch up on AI.
Carolina Milanesi, an analyst at Creative Strategies, said that misreads how consumers actually adopt technology.
"Consumers are still buying hardware first, and it's going to be like that for a long time," she said. "You're not going to discover the value of AI if you're not interested in the hardware."
Ternus earned a bachelor's degree in mechanical engineering from the University of Pennsylvania and worked as an engineer at Virtual Research Systems before joining Apple.
Inside the company he is credited with driving a push to make products more durable, reliable and resilient, and with design work that cut their carbon footprint.
The harder question is what kind of leader he becomes.
"Even people that know him now don't know him as a CEO," Milanesi said.
"You might know him as the head of engineering, but once you're CEO, things change. Your responsibility is bigger, your power is bigger. You're dancing a different kind of dance."
'Learn on the job'
Nowhere is that gap wider than in the geopolitical role Cook excelled at, courting both Beijing and Donald Trump's White House to protect a supply chain that runs largely through China.
Apple's manufacturing operation is among the most complex in corporate history, a web of hundreds of suppliers and assembly lines that Cook painstakingly built over decades.
Cook in recent years began shifting some of the work elsewhere - iPhone assembly to India, other production to Vietnam - but the diversification has been gradual with China, one of Apple's biggest consumer markets, still anchoring the system.
Complicating matters, Trump has repeatedly demanded Apple build iPhones on American soil, threatening tariffs on those made overseas.
Cook avoided the heaviest blows of Trump's trade war by cultivating the president directly, making US investment commitments and political donations - all while also keeping Beijing onside.
The tricky political terrain will be new for Ternus.
"He knows Apple Park like the back of his pocket in terms of hardware," Ives said of Ternus. "But on the global stage - that's probably one of the biggest areas where he's going to have to learn on the job."
Cook is not going far. He becomes executive chairman of Apple's board on the same day, with a mandate the company has said includes engaging policymakers around the world.
"That was really clever," said Milanesi, arguing the arrangement frees Ternus from a role Cook has handled alone for years.
The September 9 iPhone event will be the first public measure of the handover.
A foldable iPhone would be the most significant redesign in years, and Ternus will be its face - eight days into the job.
"This is a moment that they created for him," Milanesi said.
