Manager Andre Villas-Boas pushed Dempsey up front alongside Jermain Defoe on Sunday and the American repaid the Spurs manager by grabbing a dramatic 93rd-minute equalizer against a shellshocked Manchester United.
With Adebayor away in South Africa for at least Tottenham's next two games, Villas-Boas has no other option but to continue playing the American in an advanced role as he is unwilling to enter the transfer market for a short-term fix.
Adebayor had kept Dempsey out for most of the festive period, but the American is now determined to make the most of his run in the first team.
"Ade is a great player and he is going to be missed, but there is competition. You try and fight for a spot and when you get an opportunity to play you want to stand up and take advantage of that opportunity," Dempsey said following the 1-1 draw at White Hart Lane. "For me it was a slow start to the season so it's good to be chipping in with goals now and repaying the club for their belief in me. Hopefully there will be more goals to come because that's why they brought me here."
But he kept plugging away up front and combined well with Defoe before netting the last-gasp equalizer.
Dempsey is used to playing in the hole or down the left flank, but the way he popped up in the box to turn home Aaron Lennon's pass was the sign of a true goal-poaching striker.
"I can play that position," said Dempsey, who has seven goals this season. "It's a position I feel comfortable in, a position I have played a lot this season and I feel like I am starting to feel more comfortable there. Now it's about just trying to create more chances in the attacking third, whether it's getting goals or getting assists and I feel like I have been on a good run of form."
Brazil and Internacional striker Leandro Damiao has been heavily linked with Spurs, but Villas-Boas reiterated Sunday night that he does not want to sign a new forward before the transfer window shuts in the next 10 days.
The Tottenham manager, whose team next faces Leeds in the FA Cup on Sunday, has no doubt about Dempsey's ability to be a leading marksman.
"Clint is a goalscorer," Villas-Boas told Spurs TV Online. "He sniffs these opportunities like no one else. He scored two goals the other day against Coventry. He is always up there in the face of the goalkeeper. The reason why we bought him was exactly this -- his ambition to score goals."
With tough league games coming up over the next fortnight, Villas-Boas knows his team must not let its eight-match unbeaten run come to an end.
"The United game was a good reference point for us, but it does not stop here," the 35-year-old said. "We have taken a few points off Manchester United this season but it's against the other teams that you define your position in the league. We have two away games in the league now against West Brom and Norwich.
"It is going to be extremely difficult and hopefully we can continue showing these performances."