Hayden, 61, oversaw the National Security Agency from 1999 to 2005 before taking a post as the chief deputy to Director of National Intelligence John Negroponte in 2005.
"Winning the war on terror requires that America have the best intelligence possible, and his strong leadership will ensure that we do," President Bush said following the confirmation vote. "General Hayden is a patriot and a dedicated public servant whose broad experience, dedication and expertise make him the right person to lead the CIA at this critical time."
Much of the questioning during Hayden's Senate confirmation hearings dealt with two NSA programs that have been around since the Sept. 11, 2001 terrorist attacks -- monitoring overseas telephone calls originating in the United States and collecting phone records of millions of Americans.
Democrats and civil-liberty advocates have argued that the telephone call monitoring programs violate the 1978 Foreign Intelligence Surveillance Act, which requires warrants for domestic eavesdropping. But the administration has said the programs are legal and necessary to track potential terrorists.
During Thursday night's debate, Oregon Democrat Sen. Ron Wyden said Hayden's oversight of the domestic phone surveillance program raised "serious questions about whether the general is the right person to lead the CIA, serious questions about whether the general will continue to be an administration cheerleader, serious questions about his credibility."
Hayden limited his public comments about the programs, but between meetings with senators prior to the confirmation hearings, he told reporters that the NSA programs "preserve the security and liberty of the American people. Everything that the agency has done has been lawful. It's been briefed to the appropriate members of Congress."
Hayden received support from several Senate Democrats including West Virginia Sen. John Rockefeller who said Hayden could restore the CIA's credibility, praising his experience.
Hayden, a four-star general who has held many senior espionage and security positions in his 30-year military career, would be the fourth active-duty military officer to head the CIA and its first in 25 years.
Responding to criticism at his confirmation hearing, Hayden said his military status would not interfere with his ability to run the CIA, a civilian organization with no military responsibilities.
He also said he would remain independent of his military superiors at the Department of Defense.
Hayden replaces Porter Goss, who resigned in May after disagreements with Negroponte about the future of the CIA, pre-Iraq war intelligence, and the failure to prevent the Sept. 11 attacks, according to Reuters.