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Nineteen-year-old Aaron Connolly scored twice for the Seagulls on his first Premier League start after Neal Maupay had headed Brighton into an early lead.
Four days on from a 7-2 thrashing at the hands of Bayern Munich in the Champions League, Pochettino was looking for a reaction.
Instead, Spurs looked like a side devoid of confidence after getting off to the worst possible start when Hugo Lloris gifted Brighton the opener and injured himself in the process.
The France captain dropped a simple cross into the box and as he fell backwards and landed awkwardly, Maupay stooped to head into an empty net.
Lloris was stretchered off with what looked like an elbow injury and replaced by Paolo Gazzaniga.
Connolly took advantage of more generous Spurs defending and goalkeeping to double Brighton's lead before half-time and curled in his second of the day in style 25 minutes from time.
Last season's Champions League finalists have now won just three of their opening 11 games of the campaign and five of their last 19 dating back to when these sides last met in April.
And while Pochettino could justifiably claim Bayern's ruthlessness in midweek meant the scoreline was not a true reflection of his side's performance, there was no excuse for being thoroughly outplayed by a Brighton side that had not won in six league games.
The visitors' were on the back foot from the off when injury was added to insult for Lloris.
The Spurs skipper was given oxygen and morphine before being taken to hospital and now seems certain to miss France's upcoming Euro 2020 qualifiers against Iceland and Turkey.
After a lengthy delay for Lloris to be stretchered off, Brighton pushed on rather than trying to protect their lead and were rewarded just after the half hour mark.
Connolly was twice the quickest to react as he turned Dan Burn's cross goalwards and, after Gazzaniga spilled his first effort, the Irishman followed up for his first Premier League goal.
Tottenham have made a bad habit of letting leads slip in recent weeks against Arsenal, Olympiakos, Leicester and Bayern, but when forced to mount a fightback themselves were found wanting.
Pochettino sacrificed club record signing Tanguy Ndombele at half-time for Harry Winks and changed system to a 3-5-2.
However, rather than turning the tide, it was Brighton who got the third goal to kill the game off.
Connolly jinked inside onto his right foot and curled brilliantly into the far corner to round off an afternoon that he and the Seagulls will long remember.
Son Heung-min and Harry Kane then missed huge chances to pull a goal back that summed up Spurs' dire week and leaves Pochettino with plenty to ponder over the upcoming two-week international break.
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