But it also removes the biggest sceptic of an ever closer union.
Some of those who support deeper integration of the remaining 27 member states sense an opportunity, but the split could also unveil deeper fault lines masked by the Brexit storm.
For some, the decision in July at a marathon EU summit to move towards joint borrowing to fund a post-coronavirus recovery plan for the union is a sign of what can now be achieved.
“With the British, we wouldn’t even have discussed this, they’d have said ‘no’ straight away,” French professor Robert Frank, who wrote a book on Britain’s difficult European relations, told AFP.
The stimulus plan, which emerged from four straight days and nights of haggling between EU leaders, was hailed as a breakthrough by EU enthusiasts.
“It’s going to create a common fiscal policy for the EU that it hasn’t ever had before,” says Andrew Duff, a British former MEP and European federalist, now a visiting fellow at the European Policy Centre.
The joint borrowing was resisted by a coalition of so-called frugals — the Netherlands, Denmark, Austria, Finland and Sweden — who would once have counted on British support.
But, once France had convinced Germany — a long-time holdout against any EU joint debt — to get behind the plan, these smaller states were left exposed and eventually had to compromise.
“It isn’t a determined, clearly thought out strategy, but it’s a drift towards a more federal EU,” Duff argues.
In this reading, Brexit leaves France’s President Emmanuel Macron freer to push forward an agenda of deeper EU integration.
Other observers see trouble on the horizon, with the smaller, more open market economies having to speak up more against Paris and Berlin now that their British ally is gone.
“I think we’ll definitely be worse off,” says Eoin Drea, an Irish researcher for the Wilfried Martens Centre for European Studies.
There will certainly, he believes, be a “centralising focus” from France and Germany — backed by Italy and Spain — but this will be resisted by Ireland, the frugals and Eastern Europe.
Dublin will be pressured over its low corporate tax rates and the Netherlands and Sweden may find themselves faced with a bigger bill for spending on poorer neighbours.
Meanwhile, after the next seven-year budget period, eastern members like Poland and Hungary ought to have built up their economies closer to the level of their European peers.
“So they will be getting a lot less structural cohesion funds in the next budget period,” Drea said.
“How does that play out then if you’ve got these populations that have been largely heavily influenced by eurosceptic governments and populist governments in Hungary and Poland?
“You’ve got less EU money coming out and Britain performing reasonably successfully as a non-member of the EU.”
The outcome will depend on whether, as Duff believes, a future UK government will return to a close association with Brussels or whether it will eventually prosper on the outside, as Drea argues.
So where does Brexit leave Europe’s dream of becoming a geopolitical player?
Britain, like France, is a permanent member of the UN Security Council, but even as an EU member its security policy was focused on NATO and close US ties.
The EU is thus losing a powerful member, but will France find it easier to build the case for a more independent EU global strategy?
“Britain has never been in favour of the emergence of an autonomous European security strategy,” said Pierre Vimont, a former senior French diplomat and fellow of Carnegie Europe.
“Now, after Brexit, it’s exactly the moment that a ‘Europe of defence’ is starting to emerge.”
At the same time, while departing from Brussels’ embryonic security structures, Britain remains in NATO with the majority of EU members, and London still sees eye-to-eye with Paris and Berlin on many problems.
“London will want to keep a privileged relationship with France and Germany,” said Vimont, predicting the UK would “come back (in) through the window” to join the European foreign policy debate.