(Hassan Ammar ~ Associated Press)
That forces a potentially pivotal decision: Whether to bring a younger generation a step closer to ruling one of the West's most critical Middle East allies. King Abdullah has now outlived two designated successors, despite ailments of his own.
It's widely expected that the current succession order will stand and Nayef's brother, Defense Minister Prince Salman -- another elderly and ailing son of the country's founding monarch -- will become the No. 2 to the throne of OPEC's top producer.
But Prince Nayef's death opens the possibility that a member of the so-called "third generation" of the royal clan -- younger and mostly Western educated -- will now move into one of the traditional ruler-in-waiting roles as the country looks ahead to challenges such as the nuclear path of rival Iran and Arab Spring-inspired calls for political and social reforms around the Gulf.
"Saudi Arabia will have to decide if this is the time to set the next generation on the path to rule," said Simon Henderson, a Saudi affairs expert at the Washington Institute for Near East Policy.
First, however, the Saudi leadership must fall behind the successor for Nayef, the hard-line interior minister who spearheaded Saudi Arabia's fierce crackdown crushing al-Qaida's branch in the country after the 9/11 attacks in the United States. Nayef, who Al-Arabiya reported died in Geneva, was named crown prince in November after his brother Prince Sultan died.
The Allegiance Council, an assembly of sons and grandsons of the first Saudi monarch, King Abdul-Aziz, will choose the next crown prince.
The likely choice is the 76-year-old Salman, who previously served for more than four decades in the influential post of governor of Riyadh, the capital, as it grew from a desert crossroads to the center of political power for the Western-allied Gulf states.
His links to Saudi religious charities brought Salman into controversy as one of the defendants in a lawsuit by insurance companies that accused Saudi Arabia of funneling money to al-Qaida. A U.S. appeals court in New York had ruled in 2008 that the Saudi royal family and other defendants enjoy immunity from such lawsuits.
Nayef was seen as closely in tune with Saudi's ultraconservative Wahhabi religious establishment, which gives legitimacy to the royal family and strongly opposes pressures for change such as allowing women to drive or participate on Saudi's Olympic team. Salman also has little inclination to challenge the authority of the clerics or push hard for reforms, experts say.
He has long been part of the Saudi's international face -- meeting dignitaries as the Riyadh governor and military brass from the West as defense minister, including a high-profile visit to Britain in April. Neither role would be possible without nods of approval from Saudi's religious guardians.
He and Nayef also are part of an influential group known as the "Sudairi seven," sons of the late King Abdul-Aziz and wife Hussa bint Ahmad Sudairi, whose marriage helped cement the king's rule over the patchwork of tribes in Saudi Arabia.
Sami al-Faraj, director of the Kuwait Center for Strategic Studies, said impressions that Salman was less conservative than Nayef were misleading.
"The reality is there is very little difference. Both are conservative and won't rock the boat" he said. "Nayef was just a behind-the-scenes guy and Salman is more public. One was implicit; the other explicit."
The two also share a history of health issues. In 2010, Salman had spine surgery and has suffered from at least one stroke, leaving him with limited movement in his left arm, said Henderson.
Concerns about the wellbeing of the aging Saudi inner circle could encourage consideration of bringing a younger member of the royal network into the succession line, possibly as successor to Nayef as interior minister. Among the possible contenders mentioned include King Abdullah's son Mitab, the head of the National Guard, and Nayef's son Mohammad, a senior official in the interior ministry.
"Nayef's death will certainly be the biggest challenge the ruling clan faced in a few years as many are striving for the throne," said Ali al-Ahmed, a Saudi analyst at the Institute for Gulf Affairs in Washington.
President Barack Obama said Nayef "dedicated himself to the security of Saudi Arabia as well as security throughout the region."
" Under his leadership, the United States and Saudi Arabia developed a strong and effective partnership in the fight against terrorism, one that has saved countless American and Saudi lives," the White House statement added.
Nayef had been out of the country since late May, when he went on a trip that was described as a "personal vacation" that would include medical tests. He traveled abroad frequently in recent years for tests, but authorities never reported on potential ailments.
The royal family, which closely guards information about the health of its members, confirmed the death but gave no details about the cause. It said a funeral would be held Sunday after prayers in Mecca.
Soon after becoming crown prince, Nayef vowed at a conference of clerics that Saudi Arabia would "never sway from and never compromise on" its adherence to the puritanical Wahhabi doctrine. The ideology, he proclaimed "is the source of the kingdom's pride, success and progress."
Nayef had expressed some reservations about some of the reforms by Abdullah, who made incremental steps to bring more democracy to the country and increase women's rights. Nayef said he saw no need for elections in the kingdom or for women to sit on the Shura Council, an unelected advisory body to the king that is the closest thing to a parliament.
In 2009, Nayef promptly shut down a film festival in the Red Sea port city of Jiddah, apparently because of conservatives' worry about the possibility of gender mixing in theaters and a general distaste toward film as immoral.
But his top concern was security in the kingdom and maintaining a fierce bulwark against Shiite powerhouse Iran, according to U.S. Embassy assessments of Nayef.
"A firm authoritarian at heart," was the description of Nayef in a 2009 Embassy report on him, leaked by the whistleblower site WikiLeaks.
Nayef, who was interior minister in charge of internal security forces since 1975, built up his power in the kingdom though his fierce crackdown against al-Qaida after the Sept. 11 attacks and a broader campaign to prevent the growth of Islamic militancy among Saudis.
The 9/11 attacks at first strained ties between the two allies. For months, the kingdom refused to acknowledge any of its citizens were involved in the suicide airline bombings. Nayef finally became the first Saudi official to publicly confirm that 15 of the 19 hijackers were Saudis, in a February 2002 interview with The Associated Press.
Nayef took a leading role in combating the branch in Yemen as well. In 2009, al-Qaida militants tried to assassinate his son, Prince Muhammad, who is deputy interior minister and the commander of counterterrorism operations. A suicide bomber posing as a repentant militant blew himself up in the same room as the prince but failed to kill him.
Nayef's Interior Ministry allied with clerics in a "rehabilitation" program for detained militants, who went through intensive courses with clerics in "correct" Islam to sway them away from violence. The program brought praise from the United States.
Nayef was survived by several wives and 10 children.
Murphy reported from Dubai, United Arab Emirates.