It started as an informal dinner among European finance ministers more than 14 years ago and has steadily gained prominence under its veteran president, Jean-Claude Juncker.
But on Monday the grey-haired Juncker, 58, handed the reins of the Eurogroup to a polished 46-year-old Dutchman, promising a new approach to how economic policy among the 17 euro zone countries is shaped and decided.
After a 16-1 vote, the finance ministers named Jeroen Dijsselbloem, an Irish-educated social democrat with flawless English, to succeed Juncker, a Luxembourger who had headed the group for eight years. Only Spain opposed the appointment.
Juncker's departure signals the end of an era during which policy - including some of the most critical decisions of the debt crisis - was frequently discussed until the early hours of the morning over dinner and wine in a smoke-filled room.
Part of a generation of old-school politicians, Juncker disarmed but often irritated ministers with his dry sense of humor, speaking openly of having to lie about issues to the media and discussing his problems with kidney stones.
Olli Rehn, the European commissioner for economic and monetary affairs, praised Juncker as one of a kind.
"His shrewd and witty locker-room talk helped to boost morale," Rehn told a news conference as Juncker bowed out, although he will continue as Luxembourg's prime minister.
A mercurial dealmaker, Juncker was pushed to the forefront of Europe's financial firefighting when Greece revealed in 2009 that it had lied about its borrowings and run up huge debts, forcing Athens into a multi-billion-euro bailout.
Crafty and quick-witted, with a gravelly voice from heavy smoking, Juncker was always the first official to brief the media at the end of monthly Eurogroup meetings, making him one of the most prominent communicators in the EU.
But it was a tall order for a man from a country of just 500,000 people to run arguably Europe's most important decision-making body. He faced criticism in early 2011 when he told a conference in Brussels he sometimes lied, telling his audience that he favored "secret, dark debates."
Those comments fostered a sense of disarray and prompted France and Germany to favor creating a permanent, full-time post, something which has not yet come to pass. Dijsselbloem will serve for two years, although it can be renewed.
With the debt crisis calming down, the Anglophile Dutchman indicated that Eurogroup meetings might even end earlier.
"Hopefully the economic situation of the euro area will allow us to meet at normal hours, not very, very early in the morning," Dijsselbloem said.
Despite complaining of the exhaustion of the job, Juncker won credit for overseeing a series of unprecedented decisions in 2010-2012 that eventually saved Greece from insolvency and helped stem the spreading debt contagion.
"If the Eurogroup hadn't existed before the crisis, someone would have had to had invented it," said Andre Sapir, an economist at Brussels-based think tank Bruegel.
Privately, EU diplomats and officials hope Dijsselbloem, who has won plaudits for his conciliatory and straightforward style, will help restore a sense of discipline.
The meetings have at times degenerated into unstructured arguments in a room, some present have said. A session in November that failed to reach agreement on how to make Greece's debt manageable culminated in a clash between Juncker and International Monetary Fund chief Christine Lagarde.
But Dijsselbloem's relative inexperience - he had been finance minister of the Netherlands barely six weeks when his name was first floated as a Eurogroup contender - also signals that he remains reliant on Berlin to take decisions.
Germany, Europe's biggest economy and the largest donor to the euro zone's permanent rescue fund, is setting the agenda on European policymaking at a time when Germany voters are increasingly wary of bailouts for southern Europe.
"The power in elsewhere, in Berlin, and to a much lesser extent in Paris," said Paul De Grauwe at the London School of Economics. "This is going to be the same - an ineffectual Eurogroup dominated by what's decided in Berlin."
(Editing by Luke Baker)