State comptroller Manuel Galindo imposed a "sanction of disqualification from exercising public office for a period of 15 years", his institution said in a ruling made public by Capriles himself. Several thousand people attended the demonstration.
Capriles lost narrowly in the 2013 election that brought Maduro to the presidency after the death of his mentor Hugo Chavez - father of Venezuela's "socialist revolution".
The elections council, which has repeatedly favored Maduro's government, has not set a date for state governors' elections that were supposed to take place a year ago.
As the most dominant figure in the opposition over the past decade, Capriles has been at the forefront of the protests, the most combative since a wave of anti-government unrest in 2014.
Other government ministries are located there, and support for Maduro is strong among downtown residents. Officers used tear gas to force protesters to disband.
"They received us with gas and rubber bullets".
The Venezuelan president added that by raising such false claims, his opponents were attempting to lay the ground for United States military intervention in the oil-rich country.
Capriles appeared energized by the protests. She said she's thinking about joining a sister and scores of college friends who have left the South American country seeking a better future.
A demonstrator walks while building a fire on the street during a rally in Caracas, Venezuela, April 8, 2017.
Capriles reported the ban on his Twitter account.
On Thursday, one anti-government protester was killed during clashes with police.
Outraged dissidents called the shooting, which occurred at the end of daylong demonstrations in Caracas, yet another sign of the violent oppression they are subjected to under the Maduro regime. They're committing crimes and violating human rights by stepping on the rights of people.
Capriles later said his offices were damaged when gas canisters were shot through the windows, slightly injuring a custodian.
Capriles, 44, is the governor of Miranda state and a two-time presidential candidate who has become the most vocal critic of the socialist government.
Capriles said that he would appeal the decision and stay in his job as governor, which he has held since 2008.
The protests were triggered by the Supreme Court's decision to gut the opposition-controlled legislature of its last vestiges of power, a move that was later reversed after widespread worldwide condemnation and even dissent within Maduro's normally disciplined socialist leadership.
Last week, the Supreme Court issued rulings transferring the National Assembly's legislative powers to itself and revoking lawmakers' immunity from prosecution.
It drew global criticism for last week's rulings, which seized the assembly's powers and revoked lawmakers' immunity from prosecution.
Saturday's protests came after ten days of intense unrest, sparked by the Supreme Court's decision last month to strip the country's Parliament from most of its powers. But the ombudsman's office said this was not possible.
Venezuelans are dealing with the effects of a harsh economic crisis that has millions skipping meals, unable to afford soaring prices for basic goods and facing long lines for scarce products.