Retired last week after 37 years in the Army, Mr Petraeus was sworn in as the 20th director of the so-called silent service in a private ceremony.
Silent is what some in the White House want the former four-star general to remain.
Admirers and detractors alike are watching to see whether Mr Petraeus will use his influence with the media and Capitol Hill to pursue policies opposed by White House officials who disagreed with him over the course of the Afghan war.
At a time when top figures close to President Barack Obama were arguing for a troop withdrawal, Mr Petraeus helped persuade Mr Obama to increase troops in Afghanistan in a repeat of his counter-insurgency strategy in Iraq, a strategy now credited with producing tangible if fragile progress. Vice president Joe Biden, among others, wanted to leave the job to a much smaller force of trainers and special operations troops to hunt terrorists.
There is some unease among intelligence officials as Mr Petraeus assumes leadership of an organisation that has produced a series of grim assessments of conditions in Afghanistan, where the general oversaw the war directly or indirectly for more than four years.
Mr Petraeus has acknowledged differences with CIA analysts. The most recent CIA assessment of the Afghan war predicts a grim, continued stalemate in fighting with the Taliban, according to one current and one former US official, who spoke anonymously.