Following the 1-1 draw between CSKA Moscow and Bayer Leverkusen earlier on matchday five, Spurs knew a win would keep their qualification in their own hands, while a draw would leave their hopes looking slim.
But ultimately they were on the wrong end of an eventful opening to the second period as the sides traded a trio of goals in five minutes.
Monaco had already seen Hugo Lloris save Radamel Falcao's first-half penalty but their persistence was rewarded three minutes into the second half when Djibril Sidibe headed home from close range.
Harry Kane levelled matters shortly afterwards, tucking home from the spot after Kamil Glik's clumsy tug on Dele Alli, but Monaco's reply was immediate as Thomas Lemar thumped an assured left-footed finish past Lloris from a tight angle.
Try as they might, Spurs could not conjure the equaliser that would have kept them in the competition, and their meeting with CSKA at Wembley in two weeks will decide only who finishes third and claims a place in the Europa League.
Monaco, meanwhile, will head into December's draw as group winners, with their matchday six fixture against runners-up Leverkusen of little relevance.
Spurs welcomed Alli back into their starting XI and the midfielder carved out a gilt-edged opportunity as early as the sixth minute as an incisive ball caught the Monaco backline cold and sent Son Heung-min clean through, but his attempt to round Danijel Subasic was thwarted by the goalkeeper, who pushed the ball wide to safety.
Spurs ought to have been made to pay for that miss five minutes later when a succession of poor defensive clearances culminated in Eric Dier felling Fabinho with a wild swipe inside the area.
But Lloris came to his side's rescue, saving from Falcao low to his right and a double stop from Benjamin Mendy and Valere Germain followed soon afterwards as Spurs wobbled.
Monaco continued to threaten with Lemar thumping a long-range drive that was held by Lloris before Germain arrowed a low shot narrowly wide in the 35th minute.
Glik was perhaps fortunate not to receive a red card for standing on a prone Kane right in front of the referee as the half drew to a close, but the real drama began after the restart.
Sidibe put Monaco in front, thumping in a free header from six yards on the end of a cross from Mendy, who got the better of Harry Winks down the left.
Spurs' response was swift as they pulled level four minutes later, Kane succeeding where Falcao failed in converting from the spot after Alli had been hauled down by Glik.
However, Tottenham appeared to switch off straight from kick-off.
Monaco worked the ball down the right and Fabinho's cross made its way to the opposite flank and to Lemar, who had time to take a touch and drill a low effort beyond a helpless Lloris.
The France international, formerly of Monaco's local foes Nice, somehow pulled off a scarcely believable one-handed reaction save from Glik's close-range volley, a stop to rival one made against Leverkusen in a 0-0 draw on matchday three.
Lloris was at it again soon afterwards, saving impressively from Falcao but the keeper standing firm as Spurs' outstanding performer and Alli slashing a late chance wide summed up their plight as Mauricio Pochettino's side were sent crashing out.
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