The IOC said Wednesday that Carter tested positive for methylhexaneamine, a banned stimulant, in re-analysis of samples from the 2008 Beijing Olympics.
Carter and Bolt were teammates on the winning 4x100-meter team, which set a world record of 37.10 seconds. Carter ran the opening leg, and Bolt took the baton third in a team that also included Michael Frater and Asafa Powell.
"The Jamaican team is disqualified," the IOC said in a statement. "... The corresponding medals, medalist pins and diplomas are withdrawn and shall be returned."
Bolt set world record times for all three sprint titles at the Bird's Nest, establishing himself as the defining superstar of Olympic track.
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"I want to share it with my team," said Bolt said after completing his hat trick in 2008. "It's down to them that I beat the world record today. When you beat the relay world record, you feel four times happier."
Bolt and Carter will retain their gold medals from Jamaica's relay win at the 2012 London Olympics in a record time of 36.84 seconds that stands today. Bolt ran the final leg on that team.
The 31-year-old Carter has teamed with Bolt on three straight world championship relay-winning teams, from 2011 through 2015. He also took an individual bronze in the 100 in 2013 in Moscow, behind Bolt and Justin Gatlin of the US.
Carter faces a ban from the IAAF.
Trinidad and Tobago is in line to get the gold medal from 2008, Japan could be upgraded to silver, and fourth-place finisher Brazil could get the bronze medal.
The IOC's ruling states that Carter noted he was taking supplements in 2008 "advised in this respect by his coach, Mr. Stephen Francis."
"The athlete explained that he had given several samples for doping controls whilst he was taking Cell Tech and Nitro Tech before the 2008 Olympic Games and he had never tested positive for a prohibited substance," the detailed verdict stated.