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In 2000, he was involved in a tight battle for the drivers' championship with Schumacher and Häkkinen, but eventually fell out of contention into a third place finish. In 2001, he finished the year in second place, but with barely half the points (65) tallied by runaway winner Schumacher (123).

Coulthard's subsequent years at McLaren, from 2002 through 2004, were disappointing as well, as he was regularly out-paced by younger teammate Kimi Räikkönen. Many of Coulthard's critics argue that his decline began early in the new millennium. In 2003 the FIA introduced the single-lap qualifying format. Since his Formula Three days, Coulthard had the reputation of being a poor qualifier. He openly admitted that he did not like the format and was a vocal opponent of it. With the announcement that Juan Pablo Montoya was to join McLaren in 2005 alongside Räikkönen, 2004 was to be Coulthard's last year with the team. A poor tenth place finish in the final 2004 standings (24 points, equal with the injured Ralf Schumacher) had not helped Coulthard's cause for 2005 either.

In 2010 while working on air for the BBC F1 coverage, he admitted that Ferrari had approached him for a drive while he was racing with McLaren. He turned down the offer, because he realised that if he was in the lead of a Grand Prix race and Michael Schumacher was behind him, he would have to move out the way to let him through.

2005–2008: Red Bull

Red Bull Racing were attracted by Coulthard's experience and signed him for the 2005 Formula One season. He was teamed with the inexperienced Christian Klien and Vitantonio Liuzzi. Coulthard's contract at Red Bull Racing was also extended prior to the 2005 British Grand Prix, prolonging his Formula One career to at least the end of 2006.

Coulthard at the 2007 Italian Grand Prix.

For 2006, Coulthard continued at Red Bull, partnered again with Christian Klien. The team were powered by Ferrari engines, with a contract for Renault engines agreed for 2007 during the 2006 season. Technical director Adrian Newey joined the team from McLaren to design the 2007 car. These positive developments led Coulthard to state that he wished to remain with the team after the 2006 season, and to add to his victory tally with them. On 7 August 2006, the day after the Hungarian Grand Prix where Coulthard finished 5th, it was announced the he had extended his contract with Red Bull Racing for 2007 and would be teamed up with Mark Webber.

Coulthard is as of November 2011 the highest-scoring British driver ever with 535 points, beating Nigel Mansell's previous record of 482 points. At the 2006 Spanish Grand Prix he also became the 8th member of Formula One's "200 Club", joining Riccardo Patrese, Michael Schumacher, Rubens Barrichello, Gerhard Berger, Andrea de Cesaris, Nelson Piquet and Jean Alesi in the list of drivers to have started 200 Grands Prix (Alain Prost and Michele Alboreto entered 202 and 215 races but started fewer). In the 2006 Monaco Grand Prix, Coulthard scored his first podium finish with Red Bull Racing, his best result with the team and also the team's first podium finish. During the trophy presentation, Coulthard wore a red cape as the team was promoting the film "Superman Returns".

After a slow start to the 2007 season, Coulthard delivered two strong drives at the Bahrain Grand Prix and the Spanish Grand Prix where he picked up the team's first points of the season. On 6 July 2007, Red Bull Racing announced that Coulthard's contract had been extended to the end of 2008.

Coulthard driving for RBR at the 2008 Canadian Grand Prix, where he scored his second podium finish for the team

Coulthard had a bad start to his 2008 campaign after a racing incident with Felipe Massa. In a live post-incident interview with ITV's Louise Goodman, he expressed dissatisfaction with Massa's aggressive on-track behaviour.