Tehran's strikes marked a sharp escalation in pace and targets, after it had warned that any retaliation over the container ship incident would be met with a "severe response."
In recent weeks, Iran had hit Kuwait and Bahrain while avoiding Qatar since early April and the UAE since early May.
Sunday's attack on Qatar targeted a state whose mediation efforts have been central to attempts to broker a ceasefire between the U.S. and Iran - and Doha has previously said it would not act as a mediator so long as it was under attack.
The war has destabilized the Gulf, while Iran's effective blockade of the strait has caused energy prices to surge, fuelling global inflation.
Higher prices, especially for gasoline, are politically sensitive for Trump ahead of November congressional elections.
The latest flare-up cast further doubt over the future of an interim U.S.-Iranian agreement signed last month with the aim of ending the war.
On Sunday, Iran's top negotiator Mohammad Baqer Qalibaf posted on X: "The era of one-sided deals is OVER. We told you: keep your word or pay the price. Reality is knocking."
The U.S. revoked the license authorizing the sale of Iranian crude on Tuesday after Qatari and Saudi commercial tankers came under fire earlier in the week, prompting a series of tit-for-tat U.S and Iranian strikes.
While Iran has not claimed responsibility for the earlier ship attacks, analysts say Tehran uses such actions to gain leverage in negotiations.
Iran's Foreign Minister Abbas Araqchi discussed regional developments in a phone call with Pakistani Foreign Minister Ishaq Dar, whose country has been a key mediator seeking to resolve the conflict between the U.S. and Iran, Iran's semi-official Tasnim news agency reported.
The latest round of hostilities came after talks on Saturday between Araqchi and Omani Foreign Minister Badr Albusaidi in Oman.
The talks aimed at coordinating arrangements for shipping and transit in the Strait of Hormuz, Iranian foreign ministry spokesperson Esmail Baqaei said on Sunday. Legal and technical delegations from both countries discussed maritime security and safety, and agreed to continue political and technical-legal talks to reach a joint understanding, with a Qatari delegation also present, he said.
Oman's state news agency reported on Saturday that negotiators would continue talks "at the technical and political levels."
A written statement from Iran's new supreme leader, Ayatollah Mojtaba Khamenei, on Saturday threatened vengeance for the death of his predecessor and father, who was killed in the war's initial attacks.
Iran's new leader has not been seen in public since the war began.