With three players in Roy Hodgson's England World Cup squad, Pochettino's Saints had been hailed a modern success story built on an ambitious vision and a world-class academy.
It took just five years to transform Southampton from a third-tier side on the brink of bankruptcy to a top-eight Premier League club peppered with internationals playing a brand of attractive football.
While their slump to League One had been swift - only six years after reaching the FA Cup final - nobody could have predicted the speed of their ascent.
It has been a steep upwards trajectory since a Swiss billionaire businessman, the late Markus Liebherr, saved the club in 2009, and one of his daughter's Katharina is now charged with maintaining the momentum.
Pochettino's decision to quit St Mary's and move to Spurs on a five-year contract, taking with him his assistant Jesus Perez, first team coach Miguel D’Agostino and goalkeeping coach Toni Jimenez, is a blow to Southampton.
His departure has brought uncertainty - with suitors already circling around the club's best players - and is a slap in the face to fans who backed the Argentine when he was brought in to replace the popular Nigel Adkins in 2013.
SOUTHAMPTON PLAN
But the "Southampton plan" put in place by Liebherr and the club's former chairman Nicola Cortese is still in good shape. It is a plan Pochettino helped to implement, with a team largely inherited from Adkins.
"The Club has been on a constant path of growth since the arrival of Markus Liebherr in 2009," chairman Ralph Krueger said on Tuesday.
"This growth took place before Mauricio came, it continued strongly under his leadership, and it will continue into the next season."
Southampton must now act quickly to appoint a manager to steady the ship, and keep circling suitors at bay to prevent the disintegration of a team promising so much.
Two of the England camp, Adam Lallana and Luke Shaw, are being touted for moves to Liverpool and Manchester United, while Pochettino has already been linked with swoops for Jay Rodriguez and Nathaniel Clyne.
Dejan Lovren, Callum Chambers, Morgan Schneiderlin and James Ward-Prowse all flourished under Pochettino and could also be on the new Spurs' manager's radar.
HIGH-CALIBRE MANAGER
Whatever substance there is behind the transfer rumours, the Saints quickly need a strong man at the helm, who can whip the first team squad back into a unit and prevent them nervously looking for the exit.
As if answering fans' concerns directly, Krueger said: "We have begun the search for a new high-calibre manager.
"We will be looking for a manager that shares our values, our principles and our philosophy; a manager who can continue to grow the first team and build on our strong foundation – a foundation led by an ambitious vision and plan that continues to build on our world-class academy, our amazing 129-year heritage and our excellent staff, and rewards our loyal and passionate fan base."
Bookmakers installed former FC Basel manager Murat Yakin as early favourite for the Saints job. A Swiss compatriot of the club's owner, Yakin is out of work having left Basel earlier this month, and is rated an 11/4 bet to take over at St Mary's.
Former England manager Steve McLaren, ex-Liverpool boss Rafa Benitez and recent Manchester United casualty David Moyes also feature in the bookies' list of possible replacements.
(Editing by Ken Ferris)
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