The straight-talking 57-year-old replaces Jens Stoltenberg, whose decade at the helm has seen NATO grapple with Russia's war on Ukraine, China's rising might -- and Donald Trump's first term in power in Washington.
The two veteran politicians will lay a wreath at NATO's Brussels headquarters to soldiers fallen during the alliance's 75-year history, before a ceremonial Icelandic gavel is used to mark the official handover.
In opting for Rutte, a staunch US ally and stalwart backer of Ukraine, NATO's 32 nations have picked a leader expected to keep pushing support for Kyiv and efforts to bolster the alliance's own defences in the face of Russia.
"There might be nuances, changes of emphasis possibly -- but there's going to be a lot of continuity as well," a senior NATO diplomat told AFP.
- 'Whoever is on the dance floor' -
The November 5 vote in the United States represents the first major test for Rutte, and will shape his initial four-year term at the helm.
On the campaign trail, Trump has threatened not to protect NATO members who do not spend enough on defence and promised he can cut a quick deal with Russian President Vladimir Putin to end the war in Ukraine.
Rutte -- known for his astute handling of Trump -- has told fretful European countries to stop "whining" about a potential comeback for the volatile reality TV star.
"We have to work with whoever is on the dance floor," he said in February.
But the uncertainty over future Western support for Ukraine comes as Russian forces advance on the battlefield more than three-and-a-half years after the Kremlin's all-out invasion.
NATO, whose members have supplied 99 percent of all foreign weaponry to Ukraine, agreed at a summit in July to play a bigger role in delivering those arms and Rutte will be key in stewarding support.
- 'A big family' -
Another central task for Rutte will be to keep pushing NATO members to spend more on their militaries to counter any potential menace from Moscow.
Spurred on by the war in Ukraine -- and pressure from Washington -- European countries have already ratcheted up their defence spending.
This year, 23 countries are set to reach NATO's target of spending two percent of gross domestic product on their militaries.
But with the threat from Russia expected to last for years -- whatever the outcome in Ukraine -- there is a clear understanding that more will be needed.
That could prove a tough sell for Rutte -- who only saw the Netherlands reach the goal in his fourteenth, and final year, in office.
Even if he wanted to change NATO's direction, Rutte would likely struggle to shake up an alliance based on careful consensus between its members.
Stoltenberg, whose mandate was extended three times, trod a careful balancing act as NATO emerged reenergized in the face of Russia's aggression.
And the former Norwegian premier has told his successor that the greatest challenge he faces is keeping all of NATO's sometimes truculent leaders on the same page.
"That's a big family, a great family, but sometimes what is a challenge, to keep them all happy at the same time," Stoltenberg said in his final speech.
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