The Court of Arbitration for Sport ruled in favor of the seven women, who appealed the International Olympic Committee's decision to disqualify them from the Sydney Games.
The court said that International Association of Athletics Federations rules in 2000 did not allow entire teams to be disqualified because of doping by one athlete.
The IOC said the ruling was "disappointing and especially unfortunate for the athletes of the other teams who competed according to the rules."
"The IOC will continue to enforce its zero tolerance policy in the fight against doping for the sake of the athletes' health and to ensure fair competition," it said in a statement.
In Sydney, Jearl Miles-Clark, Monique Hennagan, LaTasha Colander Clark and Andrea Anderson were part of the squad that won gold in the 4x400 relay.
Chryste Gaines, Torri Edwards, Nanceen Perry and Passion Richardson were on the 4x100 bronze medal squad. All but Perry joined the appeal.
In 2007, Jones admitted she was doped in Sydney and also lost her individual golds in the 100 and 200 meters and bronze in the long jump.
"The panel found that at the time of the Sydney Olympic Games there was no express IOC or IAAF rule in force that clearly allowed the IOC to annul the relay team results if one team member was found to have committed a doping offense," CAS said.
The CAS panel of three lawyers acknowledged that the ruling might be unfair to the other relay teams that competed "with no doped athletes helping their performance."
But CAS said the ruling "exclusively depends on the rules enacted or not enacted by the IOC and the IAAF at the time of the Sydney Olympic Games."
The IOC has now lost two CAS rulings within five weeks involving Olympic medals stripped in doping cases.
Belarus hammer throwers Vadim Devyatovskiy and Ivan Tsikhan won their appeals against disqualification from the 2008 Beijing Games and regained their silver and bronze medals, respectively. Both had elevated levels of testosterone in doping controls but the CAS panel said the tests were invalid because international laboratory standards in Beijing were not respected.
The CAS inflicted a further defeat on the IOC Friday, ordering the Olympic body to pay 10,000 Swiss francs ($9,500; euro7,350) toward the athletes' legal costs.
The case was heard over two days in Lausanne, Switzerland, in May when the seven sprinters' legal team argued they should not be punished for cheating by Jones.
The panel agreed unanimously Friday that the IAAF's rule in 2000 was the decisive point.
The court also confirmed its own precedent set five years ago in a previous doping case involving U.S. relay runners at the Sydney Olympics.
That panel determined that teammates of Jerome Young should not lose their 4x400 gold medals after he was served a retroactive ban from 1999-2001 meaning he was technically ineligible to compete at the games.
Young's relay partners Michael Johnson, Antonio Pettigrew, Angelo Taylor, Alvin Harrison and Calvin Harrison won their appeal to CAS after the IAAF annulled their result.
The IAAF amended its rules in 2003 so that relay teams could then be disqualified if one member was caught doping.
Friday's ruling dashed the hopes of Jamaica's team being upgraded from silver to gold in the 4x400 relay. Russia finished third and Nigeria out of the medals in fourth.
In the 4x100, the U.S. edged France out of the medals.