On Monday, for the first time since 1958, the side led by Rob Page will play in the World Cup finals when they face the United States in Al Rayyan.
For the scores of Welsh fans arriving in Doha, wearing the now distinctive "bucket" hats, the match will be a celebration few will have experienced in their lifetime.
Yet the impact of the fixture on Wales stretches beyond the confines of the pitch, a chance to forget decades of disappointment and look towards the future, with the country's First Minister Mark Drakeford in Qatar to mark the occasion.
"Small nations have to shout very loud to get themselves heard in a global world," Drakeford told Reuters.
"There will be 5 billion homes where the World Cup will be seen in people's living rooms. Many of those will never have heard of Wales. So it's an enormous opportunity."
For a sport-loving country like Wales, where as Drakeford explains "if two flies are climbing up a wall and one of them was Welsh, people in Wales would be there supporting it", the years of missing out on the World Cup were a succession of gut punches.
Until this year, Wales's history in World Cup qualification would have given the finest Greek tragedies a run for their money as an improbable catalogue of woe.
From their failure to beat Scotland in a winner-takes all clash in the lead-up to Mexico '86 to Paul Bodin's penalty, lifted onto the bar by vengeful gods, that robbed them of a spot at USA 1994, Wales have endured more than they have enjoyed the quadrennial World Cup experience.
There were many group stage campaigns that Welsh fans will not want to remember for their unremarkable failure but there were some where the World Cup was tantalisingly dangled within reach only to be snatched away at the death.
Ahead of the 1962 tournament, they lost a playoff to Spain, they missed out on Mexico 1986 when they failed to beat Scotland and in 1994 they suffered perhaps the most crushing disappointment of all when Bodin's missed penalty against Romania left them once again out in the cold.
'THE REST IS HISTORY'
For one of Wales's greatest players, former Liverpool striker Ian Rush, that loss was the most galling of all.
"We had the full crowd at the (Cardiff) Arms Park and it was 1-1 and we missed a penalty and Romania went to the World Cup - the rest is history," he told Reuters.
"I was coming to the end (of my career) then, I was 34, and thinking 'well, I might not get another chance' and I didn't get another chance."
Rush, in Doha for an occasion he said he would have travelled anywhere to see, is finally able to enjoy the World Cup finals - which he never did as a player.
"I would go away on holiday," he said. "I would watch the quarters, the semi-final and final - I was looking to get my rest in...I was desperate to get back on the pitch. I used to go back to training early at Liverpool... I felt really frustrated so I wanted to go back and improve myself and help the players get there."
Page's players will not have to endure a similar experience.
They reached the finals by coming through the playoffs in June, largely thanks to the goals of Gareth Bale, the only player to have scored more for Wales than Rush.
They will face the US, Iran and old rivals England in Group B for a place in the knockouts.
Should they not get that far, however, there will be few Welsh tear.
"Sixty-four years since they made it," Rush said. "So this is gonna be something special for the Welsh supporters."
