"It is possible, I suppose, to imagine an extraordinary circumstance in which it would be necessary and appropriate under the Constitution and applicable laws of the United States for the president to authorize the military to use lethal force within the territory of the United States," Holder said in a letter to Sen. Rand Paul, R-Ky.
Paul had sent a letter to President Barack Obama's CIA director nominee, John Brennan, asking for the administration's views on the president's "power to authorize lethal force, such as a drone strike, against a U.S. citizen on U.S. soil, and without trial."
Paul had threatened to block Brennan's confirmation until he got an answer to his question.
Holder responded in a letter Monday that Paul made public Tuesday.
Brennan, who awaits full Senate confirmation after being cleared for the post by the Senate Intelligence Committee 12-3 Tuesday, said in a separate Monday letter to Paul the CIA had no authority to use lethal force against Americans on U.S. soil.
"If I am fortunate enough to be confirmed as CIA director, I would have no 'power' to authorize such operations," said Brennan, a 25-year CIA veteran who has most recently been Obama's top counter-terrorism adviser, overseeing the expansion of CIA and military strikes in Pakistan, Yemen and Somalia.
Paul said after receiving Holder's letter he would still filibuster Brennan's nomination.
Holder's "refusal to rule out the possibility of drone strikes on American citizens and on American soil is more than frightening -- it is an affront [to] the constitutional due process rights of all Americans," Paul said in a statement.
But Paul's promised filibuster would likely not go far because Brennan's nomination would likely get the 60 votes needed to end the filibuster, possibly as early as Thursday, The New York Times said.
Holder's letter can be found at tinyurl.com/HolderResponse. Brennan's can be found at tinyurl.com/BrennanResponse. Paul's comments can be found at tinyurl.com/PaulComments.
The attorney general's letter said, "The U.S. government has not carried out drone strikes in the United States and has no intention of doing so.
"As a policy matter, moreover, we reject the use of military force where well-established law enforcement authorities in this country provide the best means for incapacitating a terrorist threat," it said.
The United States has "a long history" of stopping terrorists through the criminal-justice system, the letter said.
"The question you have posed is therefore entirely hypothetical, unlikely to occur, and one we hope no president will ever have to confront," Holder said in his letter.
In explaining a hypothetical example, he said, "For example, the president could conceivably have no choice but to authorize the military to use such force if necessary to protect the homeland in the circumstances of a catastrophic attack like the ones suffered on Dec. 7, 1941, and Sept. 11, 2001," Holder said, referring to the World War II attack on the U.S. naval base at Pearl Harbor, Hawaii, and the terrorist attacks on the World Trade Center in New York and the Pentagon outside Washington.
Earlier in the day, the White House agreed to provide Justice Department legal documents explaining the legal rationale for targeting Americans overseas who are involved in terror-related activities that threaten the United States or U.S. interests.
Republicans have also demanded more details from the administration about the Sept. 11, 2012, terrorist attack on the U.S. diplomatic mission at Benghazi, Libya.
That attack killed Ambassador J. Christopher Stevens and three other Americans.
Sen. Lindsey Graham, R-S.C., has threatened to block Brennan's nomination until he is satisfied with the administration's responses.