John Brennan is the White House's counterterrorism adviser. (SAUL LOEB/AFP/GETTY IMAGES)

President Obama began his first term with a dramatic change of course for the CIA, issuing orders on his second day in office to close the agency’s secret prisons and ban harsh interrogation techniques.

As Obama approaches a second term with an unexpected opening for CIA director, agency officials are watching to see whether the president’s pick signals even a modest adjustment in the main counterterrorism program he kept: the use of armed drones to kill suspected extremists.

The resignation of David H. Petraeus over an adulterous affair brought an abrupt end to the short tenure of a CIA director who sought to cement the agency’s ties with the military and expand its drone fleet.

The list of possible replacements is led by three CIA veterans who have all contributed to the agency’s pronounced shift toward paramilitary operations. Obama’s choice could determine whether the trajectory continues or begins to taper off.

White House counterterrorism adviser John O. Brennan, 57, is seen by many as the leading candidate for the CIA job. In recent months, he has expressed concern within the administration that the agency has become too focused on targeted killings, even though he has presided over the sharp expansion of the drone campaign under Obama.

The other potential nominees include acting CIA Director Michael J. Morell, 54, who is regarded as a stabilizing presence more than a proponent of change, and Michael G. Vickers, 59, a senior Pentagon official who is considered the most ardent supporter of the agency’s expanded paramilitary role.

U.S. officials said Obama hasn’t signaled his choice or even when that decision might come. But senior lawmakers and agency veterans said the next director will face immediate pressure to improve intelligence gathering in places beyond those patrolled by drones.

“I think this is the time for transition,” Sen. Dianne Feinstein (D-Calif.), the chairman of the Senate Intelligence Committee, said in an interview. Counterterrorism will remain the agency’s top priority, Feinstein said, but the recent attack on U.S. compounds in Libya and mounting concerns about cyber conflicts underscore other vulnerabilities.

“We have to strengthen human intelligence in key areas,” Feinstein said, “and transition from the kind of Pakistan-Afghanistan intelligence gathering” that has dominated the agency’s agenda since the Sept. 11, 2001, attacks.

Former agency officials, including those who worked in counterterrorism, cited similar concerns over the need for a balance between paramilitary operations and intelligence collection and analysis.

“As much as there remains a terrorism threat, that can’t be the preoccupation of the director of CIA 99 percent of the time anymore,” said Bruce Riedel, a former agency analyst and adviser to Obama. The fundamental question for Obama, Riedel said, is: “Should the agency be looking to be the principal player in a global drone war versus its more traditional role as the principal collector and analyst of foreign intelligence?”

CIA officials have argued in recent years that the agency can do both without erosion in the quality of its analytic work on other subjects. Before his resignation, Petraeus had made adjustments to CIA deployments overseas to bolster its presence in Africa and the Middle East, officials said.

Although Petraeus’s sudden departure stunned the agency’s workforce, current and former U.S. officials said the impact was muted by the retired general’s relatively short tenure and a perception that he struggled to connect with the rank and file.

“I think Petraeus never really caught on,” said a longtime CIA officer who met regularly with Petraeus and spoke on the condition of anonymity to speak freely. “People are sympathetic. I don’t know that there’s a whole lot of mourning.”

The agency has grown accustomed to sudden departures from a job that doesn’t come with a fixed term like its FBI counterpart. Obama now faces the task of filling the position for the third time since he became president, a turnover rate that exceeds any other slot on his national security team.

Morell is in his second stint as acting director, after serving in that capacity for several months after Leon E. Panetta left to run the Pentagon and before Petraeus arrived last year.

A career intelligence analyst, Morell is known for a sharp mind and smooth presence in meetings at the White House or on Capitol Hill. Bespectacled and bookish, Morell served as the daily briefer to President George W. Bush in 2001 and 2002, which meant he played a key role in the aftermath of the Sept. 11 attacks but was also a conduit for the erroneous intelligence on Iraq’s alleged weapons stockpiles before that war.

Morell “is one of those people who just immediately impresses you with their intellect” but is more manager than visionary, said a former colleague. “What he would signify as director is ‘steady as she goes.’ ”

Vickers, now undersecretary of defense for intelligence, is seen as the potential CIA candidate most closely identified with the convergence of the agency and the military. A former Army special operations soldier and CIA analyst, Vickers helped arm mujaheddin fighters in Afghanistan in the 1980s as part of the U.S. effort to drive Soviet forces out of the country. In his most recent assignments at the Pentagon, Vickers has fostered deeper collaboration between the CIA and the Joint Special Operations Command.

None of the likely candidates responded to requests for comment. The White House also has declined to comment on a replacement for Petraeus.

Because of Brennan’s close relationship with Obama, he is thought to have the inside track on the job. A veteran of 25 years at the CIA, Brennan was widely expected to be nominated as director four years ago. He backed out after being criticized by liberal groups for his links to the controversial counterterrorism programs of the Bush administration, including “enhanced interrogations.”

Feinstein said she believes Brennan would win Senate confirmation if he were nominated, but she also said “the position is in very good hands” with Morell.

Whether Brennan still wants the job is another question. In recent months, he has signaled to colleagues that he might step down after four grueling years in the White House.

Brennan has sought to impose more scrutiny on the selection of targets for drone strikes and has privately voiced concern that the CIA has strayed too far from its core mission of intelligence gathering, U.S. officials said.

But during Brennan’s tenure in the White House, the drone campaign accelerated in Pakistan and spread to Yemen. “It’s hard to see how the architect of the drone campaign would come in and dismantle it,” a former senior CIA official said.

Julie Tate contributed to this report.