The collision left a breach about 10 feet by 10 feet (three by three meters) in the starboard side of USS Porter. No one was injured on either vessel, the U.S. Navy said in a statement.
The collision with the Panamanian-flagged and Japanese-owned bulk oil tanker M/V Otowasan happened about 1 a.m. local time. Photos released by the Navy showed workers standing amid twisted metal and other debris hanging down from the hole.
The cause of the incident is under investigation, the Navy said, though the collision was not "combat related." There were no reports of spills or leakages from either the USS Porter or the Otowasan, the Navy said. The USS Porter was heading to the nearest port to assess the damage.
The USS Porter is on a scheduled deployment to the U.S. 5th Fleet, which is based in Bahrain, an island nation in the Gulf, near Iran.
The Strait of Hormuz, at the mouth of the Gulf, is a crowded and tense waterway where one-fifth of the world's oil is routed. Tensions have risen there over repeated Iranian threats to block tanker traffic in retaliation for tighter sanctions by the West. The sanctions are aimed at persuading Iran to abandon its uranium enrichment program, so far without success.
Tensions in the Strait of Hormuz show no sign of abating.
The United States stoked the flames recently with an announcement that it will send U.S. Navy minesweepers and warships into the Gulf for exercises. The U.S. military maneuvers scheduled for September, to be joined by ships from about 20 American allies.
This is part of a Pentagon buildup in the Gulf with more troops and naval firepower, seeking to rattle Iran and reassure Saudi Arabia and Washington's other Gulf Arab partners worried about Iran's influence and power.
Iranian commanders and political leaders have stepped up threats and defiant statements in recent weeks over the Strait of Hormuz.
While it appears unlikely that Iran is ready to risk an almost certain military backlash by trying to close Hormuz - which is jointly controlled with Oman - the comments from Tehran show that Iranian authorities see the strait as perhaps their most valuable asset in brinkmanship over tightening sanctions.
Iranian officials have been quick to counter statements about closing the strait with observations that the situation is not likely to become that severe, indicating recognition that a step like closing the strait would have grave implications.
Warnings from Tehran in the past about possible closure have been enough to boost oil prices to offset the blow of sanctions. It's also among the potential flashpoints if military force is used against Iran over its nuclear program.
If attacked, Iran could severely disrupt oil supplies and send the shaky global economy stumbling backward again.
Three years ago, The USS Hartford, a nuclear-powered submarine based in Groton, Conn., collided in the strait with the USS New Orleans, a San Diego-based amphibious ship.
The New Orleans' fuel tank was ruptured, and 15 sailors on the Hartford suffered minor injuries. The collision caused $2.3 million in damage to the New Orleans, and the cost so far of repairs to the Hartford is $102.6 million.
The submarine's commanding officer was relieved of his duties, and the sub's chief of the boat, an adviser to the commanding officer, was reassigned. Several crew members were punished.