He appeared before a Paris judge on Thursday and was formally charged in connection with the December 2007 killing of two undercover Spanish police officers in southwestern France's Landes region.
Txeroki is accused of helping prepare the murder, but officials said there was no evidence to prove that he was the third man who gunned down the two men as they stepped out of a cafe.
He was charged with "leading a criminal group with terrorist aims", an offence punishable by 20 years in prison.
Theft charges
Spanish officials had described Txeroki as the most important Eta leader still at large and the head of the group's armed wing.
Spain went on terror alert following his arrest, and Alfredo Perez Rubalcaba, the interior minister, said his capture marked a considerable blow against the organisation.
In the case of the 2007 attack on the Spanish police officers, Txeroki was charged with stealing weapons and vehicles and with possession of bomb-making materials, but he was not indicted for murder.
Leire Lopez Zurrutuza, 31, Txerori's alleged lieutenant, was also charged with taking part "in a criminal enterprise with terrorist aims" on Thursday and both were remanded in custody.
Eta, which has killed more than 820 people in its 40-year campaign for an independent Basque homeland, claimed responsibility for the December 1 attack in a statement issued two weeks after the incident.
Earlier this week, France said it was ready to hand Txeroki over to Spain.
Special accord
The two countries have stepped up co-operation in cracking down on Eta since a special accord was signed in January 2008 allowing Spanish agents to operate freely in southwestern France.
France began arresting Eta suspects after the group called off a 15-month-old ceasefire in June 2007, breaking hopes of a peace settlement.
Michele Alliot-Marie, the French interior minister, said 36 people who were either Eta members or linked to the group had been arrested in France since the beginning of the year.
Txeroki's arrest was the biggest blow against Eta since the group's presumed leader, Javier Lopez Pena, was detained along with three other suspected members of the group in France in May.
Spanish police believe Txeroki is connected to all the major Eta operations carried out since late 2003 when he is alleged to have taken over the group's military operations.
He is linked to a Madrid airport bomb attack in December 2006 that killed two Ecuadorian men and led the socialist government of Jose Luis Rodriguez Zapatero, Spain's prime minister, to end its tentative peace talks with Eta.