For the administration, Wednesday served as a reminder that the world does not operate in the black-and-white terms that Mr. Trump used on the campaign trail and on Twitter, one in which the Sunni-dominated Islamic State and Shiite Iran are part of a continuum of “radical Islamic extremism.”

“This is an illustration of the competing priorities and contradictions facing this administration, which will prove hard to reconcile,” said Robert Malley, the top Middle East policy official for the Obama administration. “You can’t be all-out against Iran, all-out against ISIS and terrorism, and maintain ‘America First’ — another way of saying keeping a light footprint in the region.”

Just a day earlier, on Tuesday, Mr. Trump posted a series of tweets taking credit for Saudi Arabia’s move to isolate Qatar and appearing to ally with Riyadh. The president also asked King Salman of Saudi Arabia in a call to draw up a list of grievances for Qatar to address, according to a senior administration official.

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Defense Secretary James Mattis was greeted by military dignitaries as he arrived at Al Udeid Air Base in Qatar in April.

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Jonathan Ernst/Reuters

That call followed several by Secretary of State Rex W. Tillerson, who knows the Sunni gulf leaders from his days as chief executive of Exxon Mobil. He asked Saudi officials to list the demands they want Doha to meet in return for an end to the dispute, and lift a newly imposed embargo against Qatar by Saudi Arabia, Egypt and several other states.

Inside the administration, Mr. Tillerson and Defense Secretary Jim Mattis repeatedly noted that the United States could not afford a rupture between Saudi Arabia and Qatar. There are roughly 11,000 American troops at Al Udeid Air Base, outside Doha, where the air war against the Islamic State is managed.

The Qataris were shocked at the contradiction between evenhanded statements from the State Department and Pentagon, and Mr. Trump’s tweets castigating the tiny Gulf state. They began asking American officials whether their longtime alliance was in peril.

By Wednesday, Mr. Trump offered to invite both sides to the White House and suggested Mr. Tillerson as a mediator. The president also called the Qatari emir, Sheikh Tamim bin Hamad Al-Thani, to repeat his urgings on Twitter to cut off financing of extremist groups. While Qatar’s support for those groups — including the Muslim Brotherhood, which the Saudis and the Egyptians consider a serious threat — is without question, the same charge could be leveled at the Saudis, who have allowed funds to flow to other Sunni extremists.

Analysts said Mr. Trump’s public support for Saudi Arabia emboldened the kingdom and sent a chill through other Gulf states, including Oman and Kuwait, that fear that any country that defies the Saudis or the United Arab Emirates could face ostracism as Qatar has.

“Everyone in the region is looking over their shoulder, thinking, ‘This is potentially us,’” said Gerald M. Feierstein, a former ambassador to Yemen who was the State Department’s second-ranking diplomat for Middle East policy from 2013 to 2016.

Mr. Feierstein, now the director for gulf affairs at the Middle East Institute, said that “the bottom line for us is, we have to come out of all this with a consensus on combating terror finance and not blowing the G.C.C. to smithereens,” he said, referring to the Gulf Cooperation Council, the loose association of Sunni Arab states.

Among the Saudi complaints about Qatar — mostly that it finances extremists and hosts Al Jazeera, the Arab news channel that is frequently critical of the Saudis — is its episodic cooperation with Iran. That may add to Mr. Trump’s suspicions about Qatar.

Ultimately, Mr. Trump told the Saudi and Qatari leaders that the campaign against the Islamic State would be more effective with a unified alliance. Mr. Trump also spoke on Wednesday with Sheikh Mohammed bin Zayed Al-Nahyan, the crown prince of Abu Dhabi in the U.A.E., underscoring G.C.C. unity to promote regional stability, “but never at the expense of eliminating funding for radical extremism or defeating terrorism,” according to an administration statement.

Mr. Trump’s hesitant response to the terrorist attack in Iran underscored that the hurdles to pursuing a unified strategy come from Washington as well.

The Trump administration is divided about how to deal with Tehran, and two White House reviews of Iran policy have been grinding ahead for weeks.

The carefully bifurcated White House statement about the onslaught in Iran, which killed 12 and wounded 46, was issued shortly before 4 p.m. in Washington. More than three hours earlier, the State Department issued its own statement to stoutly condemn the attacks.

“We express our condolences to the victims and their families, and send our thoughts and prayers to the people of Iran,” said a State Department spokeswoman, Heather Nauert. “The depravity of terrorism has no place in a peaceful, civilized world.”

One faction in the National Security Council has been pressing to find ways to sanction Iran, hoping to reimpose economic penalties against Tehran that were lifted after the 2015 nuclear agreement between world powers and the Islamic republic. But that strategy risks blowing up the accord, which others in the administration — including Mr. Mattis and the national security adviser, Lt. Gen. H. R. McMaster — want to preserve to keep Iran from quickly developing a nuclear weapon. To date, Iran has complied with the agreement.

But there appears to be no chance, administration officials say, that the Trump administration will try to find common cause with Tehran on fighting the Islamic State. Nor does there appear to be a strategy yet for managing the growing competition between Saudi Arabia and Iran for dominance of the Middle East.

The result is that while the Trump administration now finds itself in the middle of the Saudi-Qatari dispute, it may soon find itself caught between the Saudis and Iran. On Wednesday, Tehran accused the Saudis of likely being behind the terrorist attack against the Parliament in Tehran, despite no evidence of such responsibility so far.

“It’s in U.S. interests to try and compel Tehran and Riyadh to address their differences and cooperate against ISIS,” said Karim Sadjadpour, a senior fellow in the Middle East Program at the Carnegie Endowment for International Peace. “Acrimony and distrust between Iran and Saudi Arabia only causes more civilian casualties in Syria and Yemen, more refugees pouring into Europe, and more Sunni and Shia radicalism.”

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