Only weeks after ending their English Premier League campaign with a club-record 56 points, Saints find themselves managerless and on the cusp of an exodus threatening to rip the heart out of one of last season's most exciting teams.
The 32-year-old could be confirmed a Liverpool player within 48 hours, local media reported, as the Reds want the deal wrapped up before he flies to Miami with England on Monday to continue World Cup preparations.
The news of Lambert's impending move came on the day Southampton reminded fans of their deadline to renew season tickets for St Mary's stadium.
A Twitter reminder of the May 30 deadline was peppered with replies from fans - some ironic, most abusive - as they came to terms with the reality of a disintegrating team.
"Yet again, roll over, and get our belly tickled. Embarrassed..." one fan posting as BracknellSaint wrote on Southampton newspaper the Daily Echo's website.
"...totally cheesed off with #SaintsFC," another fan calling himself Saintjeff posted on Twitter. "Joke Club, Joke Management. Other Clubs tearing us up".
Lambert's record of a goal every other game for Southampton (114 in 228 appearances) speaks for itself, and he will be sorely missed on the pitch.
He rattled in 13 league goals for the Saints last season as they finished eighth in the table, forcing his way into Roy Hodgson's World Cup squad at the same time.
But it is the broader signal his departure would make which is most worrying for supporters.
While few would begrudge him this move at this stage in his career - a move to Anfield would be a dream come true for the Liverpool-born player who was released by his hometown club at the age of 15 - the loss of the striker will be a bitter blow to a club reeling from manager Mauricio Pochettino's departure this week.
The Argentine left Saints for the deeper pockets of Tottenham Hotspur and Lambert's exit will further rock the destabilised South Coast side.
Fans had been braced for skipper Adam Lallana and left-back Luke Shaw to leave over the summer. Both also feature in England's World Cup squad and Lallana is also a target of Liverpool, while Manchester United are linked with a move for Shaw.
Worse news could be in store for the managerless club, however, as Pochettino is said to be keen on taking another England Saint Jay Rodriguez to Spurs, while suitors are circling around defenders Nathaniel Clyne and Dejan Lovren - the latter being the third Southampton player to be linked with Liverpool.
As British media whipped itself into a frenzy regarding further transfer speculation at the south coast club, the Daily Mail reported that Saints' Kenyan midfielder Victor Wanyama wants to follow Pochettino to Spurs.
The Southampton board this week spoke of acting swiftly to replace Pochettino with a top-notch manager, but until they do so there appears little the club can do to stem this PR disaster.
Feyenoord head coach Ronald Koeman was the latest big name to be linked with the club after his agent told Southampton newspaper the Echo that the 51-year-old former Dutch international would be keen to discuss the vacancy.
But the new man - whether it be Koeman, ex-Basel coach Murat Yakin or somebody closer to home - may find himself with only the bare bones of a team unless they can find a way to halt an impending exodus in its tracks and repel the cash being thrown at them by the Premier League's big spenders.
- Sports & Recreation
- Premier League