The guidelines confirm the EU's top three priorities are to guarantee the rights of EU and UK citizens, settle the UK's financial obligations and avoid a hard Irish border.
While it took all of 60 seconds to agree the guidelines, or 'red lines', for the upcoming Brexit talks, the EU leaders and heads of state will be all too aware that the apparent show of unity may start to fray once the serious negotiations finally begin.
Signs of this started to appear soon after the summit when German newspaper Frankfurter Allgemeine Zeitung reported that European Commission President Jean-Claude Juncker believes there is an over 50 per cent chance that Brexit talks could collapse.
He is alleged to have made the comments following a dinner in London with Prime Minister Theresa May last Wednesday.
According to the German newspaper's report of the dinner , which allegedly came via European Commission sources, after May said she wanted to "make Brexit a success", Juncker's response was, "Brexit cannot be a success. The more I hear, the more sceptical I become."
When she said the UK owes no money to the EU, Juncker is said to have informed her that she was not leaving a "golf club".
Another EU diplomat told The Sunday Times newspaper, "The UK's position is miles apart, both on their financial obligations and on the EU citizens' rights."
On Monday, however, a spokesperson for May said she had dismissed the account as "Brussels gossip".
The row over who said what comes after the EU agreed its negotiating strategy on Saturday.
"Guidelines adopted unanimously. EU27 firm and fair political mandate for the Brexit talks is ready," Council President Donald Tusk tweeted while EU leaders burst into applause when the guidelines were waved through.
Meeting for the first time since British Prime Minister Theresa May formally triggered a two-year countdown to Brexit in late March, the 27 other EU leaders took just a minute as they sat down to lunch in Brussels to approve eight pages of negotiating guidelines hammered out by their diplomats, or sherpas as they are known, over the past month.
These will bind Michel Barnier, the EU's chief Brexit negotiator, to seek an agreement that secures the rights of three million EU expats living in Britain, ensure London pays tens of billions of euros Brussels thinks it will be owed and avoids destabilising peace by creating a hard EU-UK border across the island of Ireland.
One of the thorniest issues is the size of the divorce bill with EU officials estimating that the UK faces a bill of €60bn because of EU budget rules. UK politicians have said the government will not pay a sum of that size.
Ireland is another potential obstacle to any deal. Britain will be reminded in the coming weeks to abide by the terms of the 1998 Good Friday agreement, including keeping the door open to the possible unification of Ireland. EU leaders have also reiterated that they will rule out discussing the free trade deal May wants until they see what has been called "sufficient progress" on agreeing those key withdrawal terms.
Antono Tajani, President of the European Parliament, which must sign of any Brexit deal, said, "For Parliament, 'orderly withdrawal' means, above all, finding a quick solution to the problem of EU citizens resident in the UK and British citizens resident in the EU.
"There will be difficult moments. Unity will be our strength and our greatest asset. Our citizens have placed their hopes in us. They are looking to us to defend their interests and to show that we are up to the task which we have been given."
Afterwards, Tusk commented, "We all want a close and strong future relationship with the UK. There is absolutely no question about it. But before discussing the future, we have to sort out our past. We will handle it with genuine care, but firmly. This is, I think, the only possible way to move forward.
"We also need solid guarantees for all citizens and their families who will be affected by Brexit, on both sides. This must be the number one priority for the EU and the UK. And the Commission has already prepared a precise and detailed list of citizens' rights we want to protect."
The Polish official went on, "We need to remain united as EU27. It is only then that we will be able to conclude the negotiations. Our unity is also in the UK's interest. And as for now, I feel strong support from all the EU institutions, including the European Parliament, as well as all the 27 member states. I know this is something unique, but I am confident that it will not change."
Talks with the UK will now begin after the UK general election on 8 June. The deadline for completing the negotiations is 29 March 2019.
That the guidelines approved on Saturday have not changed all that much in the past month shows that the EU's claim to have a unified position on Brexit is more than skin deep.
European leaders are emboldened by mostly positive economic news in recent months and by the defeats of ferocious opponents of the bloc in elections in Austria and The Netherlands. Europeans are also broadly optimistic that Emmanuel Macron, the centrist candidate in the French presidential elections, will prevail over Marine Le Pen of the far-right National Front in the final round on 7 May.
Since May triggered two years of talks in March, she has seemed to dilute her stance on several occasions and the British are deemed to have made concessions on several key matters involving finance, trade and immigration.
This partly explains why EU officials are increasingly hopeful that May will realise that the terms of Brexit will be set by them more than her.
Crucial issues to be discussed now include what criteria they may use to judge, come the autumn, whether the two sides have made "sufficient progress" on the terms of the UK divorce settlement to warrant a start on trade talks. EU leaders may also talk about how to manage a transition, after Britain leaves in 2019, to a new relationship likely to take many more years to finalise.
A decision on what is "sufficient progress" is the kind of debate that can poison relations as the 27 seek to protect national interests.
Also contentious will be which countries scoop the prizes of hosting the European Medicines Agency and the European Banking Authority, the two EU agencies set to be moved from London.