Under a deal reached by the 28 member governments on Tuesday after long and fraught negotiations, Von der Leyen, an ally of German Chancellor Angela Merkel, will replace Jean-Claude Juncker as head of the EU's executive Commission.
France's Christine Lagarde will head the European Central Bank..
Leaders hope the decision to put two women at the top of EU decision-making for the first time will send a positive message and repair damage to the bloc's image wrought by such a fractious summit, diplomats said.
The discord echoed a wider fracturing of the EU's political centre evident in May's elections to the European Parliament, which delivered a more fragmented assembly with bigger far-right and far-left contingents.
"In the end, we've got a package that found unanimity and that's a very important achievement," said a senior EU diplomat, who asked not to be named.
"It's the eternal compromise, but that's how we work ... The parliament will make its peace with it. They'll huff and puff, as they do. But they’ll back it in the end."
Yet the selection wrangles could portend difficulties ahead for Von der Leyen, currently German defence minister, as she tries to marshal a strong and united EU response to issues from global warming and Brexit to trade wrangling with Washington and Iran's nuclear ambitions.
Von der Leyen needs to be confirmed in her new job by an absolute majority of the 751 EU lawmakers.
"I decided that my very first stop would be here in Strasbourg to meet the European Parliament ... because here is where the heart of the European democracy is beating," she told reporters at the legislature.
She said her hope was to nurture "intensive cooperation" between the European Commission, European Council of national leaders, and European Parliament over her five-year term.
On paper, Von der Leyen ought to be able to secure those votes comfortably, but she may hit resistance in an assembly aggrieved that EU leaders ignored the lead candidates from the main parliamentary blocs - the "Spitzenkandidaten" - in their horse-trading over top posts.
PARLIAMENT GETS ITS MAN
The parliament did, however, get its wish on Wednesday to choose its own preferred candidate as speaker for the next 2-1/2 years, something that may smooth ruffled feathers.
Italian socialist David Sassoli, a 63-year-old former journalist who has served for 10 years as an EU lawmaker, was elected after two rounds of voting.
The Socialist and Green groupings had been particularly upset at Von der Leyen's nomination.
"This backroom stitch-up after days of talks is grotesque, it satisfies no one but party power games," said Greens leader Ska Keller.
The Socialists' leader in the assembly, Spain's Iratxe Garcia, called the agreement "deeply disappointing".
They were mostly angered by east European leaders' rejection of socialist Frans Timmermans as Commission head, a move that many saw as retaliation against his accusations of civil rights violations in Hungary and Poland.
Von der Leyen can, however, rely on the support of the main centre-right and liberal groupings. Another conservative group led by Poland's ruling PiS party also looks set to back her.
Most Italian lawmakers, although eurosceptic, are also likely to support Von der Leyen, after Italian Prime Minister Giuseppe Conte welcomed the deal on her nomination.
This would give her enough votes to be endorsed, even without the backing of the socialists.
Under the deal reached by the EU leaders, and backed by conservatives, the centre-right will have the presidency of the parliament in the second half of the five-year legislature.
While a gender balance has been maintained in choosing the EU's top posts, the East-West balance has been neglected, with no eastern European designated for a top position.
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