Issuing English-language sermons on jihad on the Internet from his hideouts in Yemen's mountains, al-Awlaki drew Muslim recruits like the young Nigerian who tried to bring down a U.S. jet on Christmas and the Pakistani-American behind the botched car bombing in New York City's Times Square.
Friday's drone attack was believed to be the first instance in which a U.S. citizen was tracked and killed based on secret intelligence and the president's say-so. Al-Awlaki was placed on the CIA "kill or capture" list by the Obama administration in April 2010 - the first American to be so targeted.
The strike took place in the morning hours in the eastern Yemeni province of al-Jawf. A second American, Samir Khan, who edited al-Qaida's Internet magazine, was also killed in the airstrike.
Late Friday, two U.S. officials said intelligence had indicated that the top al-Qaida bomb-maker in Yemen also died in the strike - Ibrahim al-Asiri, who was linked to the bomb hidden in the underwear of the Nigerian man accused of trying to blow up a plane over Detroit on Christmas Day 2009.
The officials spoke on condition of anonymity because al-Asiri's death has not officially been confirmed. Al-Asiri is also believed to have built the bombs that al-Qaida slipped into printers and shipped to the U.S. last year in a nearly catastrophic attack.
Christopher Boucek, a scholar who studies Yemen and al-Qaida, said al-Asiri was so important to the organization that his death would "overshadow" the news of the deaths of al-Awlaki and Khan.
Khan published a slick English-language Web magazine, "Inspire," that spouted al-Qaida's anti-Western ideology and even offered how-to articles on terrorism - including one titled, "Make a Bomb in the Kitchen of Your Mom."
The voices of Khan and al-Awlaki elevated the several hundred al-Qaida fighters hiding out in Yemen into a greater threat than similar affiliates of the terror network in North Africa, Somalia or east Asia.
President Barack Obama heralded the strike as a "major blow to al-Qaida's most active operational affiliate," saying the 40-year-old al-Awlaki was the group's "leader of external operations."
"In that role, he took the lead in planning and directing efforts to murder innocent Americans," Obama told reporters in Washington, saying al-Awlaki plotted the Christmas 2009 airplane bombing attempt and a foiled attempt in 2010 to mail explosives to the United States.
Al-Awlaki's death was the biggest success in the Obama administration's intensified campaign to take out al-Qaida's leadership since the May killing of Osama bin Laden in Pakistan. The pursuit of al-Awlaki and Friday's strike were directed by the same U.S. special unit that directed the Navy SEALs raid on bin Laden's hideout.
After three weeks of tracking the targets, U.S. armed drones and fighter jets shadowed al-Awlaki's convoy, before drones launched the lethal strike early Friday, U.S. officials said, speaking on condition of anonymity to discuss matters of intelligence.
Al-Awlaki and his comrades were moving through a desert region east of Yemen's capital near the village of Khasaf between mountain strongholds in the provinces of Jawf and Marib when the drone struck, U.S. and Yemeni officials said.
A tribal chief in the area told The Associated Press that the brother of one of those killed witnessed the strike. The brother, who had sheltered the group in his home nearby, said the group had stopped for breakfast in the desert and were sitting on the ground eating when they saw the drone approaching. They rushed to their truck to drive off when the missiles hit, incinerating the vehicle, according to the tribal chief, who spoke on condition of anonymity because he did not want to be associated with the incident.
U.S. officials said two other militants were killed in the strike. But the tribal chief, who helped bury the bodies in a Jawf cemetery, said seven people were killed, including al-Awlaki, Khan, two midlevel Yemeni al-Qaida members, two Saudis and another Yemeni. The differing numbers could not immediately be reconciled.
Al-Awlaki, who was born in New Mexico to Yemeni parents, had been in the U.S. cross-hairs since his killing was approved by Obama last year. At least twice, airstrikes were called in on locations in Yemen where al-Awlaki was suspected of being, but he wasn't harmed.
In July, U.S. Defense Secretary Leon Panetta said al-Awlaki was a priority target alongside Ayman al-Zawahri, bin Laden's successor as the terror network's leader.
Bruce Riedel, a Brookings senior fellow and former CIA officer, cautioned that while al-Awlaki was the "foremost propagandist," for al-Qaida's Yemen branch, his death "doesn't really significantly change its fortunes."
Al-Qaida's branch "is intact and arguably growing faster than ever before because of the chaos in Yemen," he said.
Al-Qaida in the Arabian Peninsula, as the terror branch in Yemen is called, has been operating in Yemen for years, led by a Yemeni militant and former bin Laden aide named Nasser al-Wahishi. Its main goal has been the toppling of Yemeni President Ali Abdullah Saleh and targeting the monarchy in neighboring Saudi Arabia, and its several hundred militants have found refuge among tribes in Yemen's mountainous regions, where the Sanaa government has little control.
Amid the past seven months of political turmoil in Yemen, al-Qaida and other Islamic militants have gained even more of a foothold, seizing control of at least three towns and cities in the south and battling with the army.
Al-Wahishi placed major importance on propaganda efforts.
In the latest issue of Inspire, put out earlier this month, Khan - a U.S. citizen of Pakistani heritage - recounted meeting the Yemeni al-Qaida leader. "'Remember,' he said, as other mujahedeen were busy working on their computers in the background. 'The media work is half of the jihad,"' Khan wrote.
Al-Awlaki gave the group its international voice.
He was young, fluent in English, well-acquainted with Western culture and with the discontent of young Muslims there. His numerous video sermons, circulated on YouTube and other sites, offered a measured political argument - interspersed with religious lessons - that the United States must be fought for waging wars against Muslims.
Downloads of his sermons were found in the laptops and computers of several groups arrested for plotting attacks in the United States and Britain.
Al-Awlaki exchanged up to 20 emails with U.S. Maj. Nidal Malik Hasan, accused of opening fire at the U.S. military base at Fort Hood, Texas, killing 13 people, in a 2009 rampage. Hasan initiated the contacts, drawn by al-Awlaki's Internet sermons.
Al-Awlaki has said he didn't tell Hasan to carry out the shootings, but he later praised Hasan as a "hero" on his website.
In New York, the Pakistani-American who pleaded guilty to the May 2010 Times Square car bombing attempt told interrogators he was "inspired" by al-Awlaki after making contact over the Internet.
But U.S. officials say al-Awlaki moved beyond being just a mouthpiece into a direct operational role in organizing such attacks as he hid alongside al-Qaida militants in the rugged mountains of Yemen.
Most notably, they believe he was involved in recruiting and preparing Umar Farouk Abdulmutallab, the Nigerian who tried to blow up a U.S. airliner heading to Detroit on Christmas 2009, failing only because he botched the detonation of explosives sewn into his underpants.
Yemeni officials say they believe al-Awlaki and other al-Qaida leaders met with Abdulmutallab in a Yemen hideout in the weeks before the failed bombing. Al-Awlaki has said Abdulmutallab was his "student" but said he never told him to carry out the airline attack.
Al-Awlaki began as a mosque preacher as he conducted his university studies in the United States, and he was not seen by his congregations as radical. While preaching in San Diego, he came to know two of the men who would eventually become suicide-hijackers in the Sept. 11, 2001, attacks on the World Trade Center and the Pentagon. The FBI questioned al-Awlaki at the time but found no cause to detain him.
In 2004, al-Awlaki returned to Yemen, and in the years that followed, his English-language Internet sermons increasingly turned to denunciations of the United States and calls for jihad, or holy war. Since the Fort Hood attack, he has been on the run alongside al-Qaida militants.
U.S. terrorism expert Evan Kohlmann said al-Awlaki's death doesn't affect al-Qaida in the Arabian Peninsula's military capabilities. "The one area it makes a difference is, it limits the ability of AQAP to put out more English-language propaganda," at least in the short term.
"Al-Awlaki's greatest importance really is a recruiter for homegrown terrorism," he said. "There is no doubt he has provided assistance to recruiting people on behalf of AQAP."
But Kohlmann noted that al-Awlaki's sermons and calls for jihad remain on the Web and "in some ways you could say they may be even more effective now because he has been martyred for his cause. ... That is a powerful lesson."
AP correspondents Matt Apuzzo, Adam Goldman, Lolita Baldor and AP Intelligence Writer Kimberly Dozier in Washington and Lee Keath and Sarah El Deeb in Cairo contributed to this report.