The 60- to 70-foot-long fishing vessel collided with the USS Lake Champlain -- a 568-foot Ticonderoga-class guided missile cruiser that has been with the aircraft carrier USS Carl Vinson strike group.
No injuries were reported and damage assessments for both ships are underway, according to a Navy press release.
"It's very common" to have small boats come up close, a Navy official told CNN, adding that there were no guns displayed or obvious signs of hostile intent in Tuesday's incident.
The fishing vessel crew later said it didn't have a radio and didn't hear the radio calls from the Navy, according to the official.
While Navy officials are downplaying the collision, former sailors said that incidents of this kind are not "commonplace," as the service suggested and, at the very least, represent a significant professional embarrassment.
"At end of the day, this is unacceptable. It is not considered a fact of life in (the) maritime community," said Bryan McGrath, a Navy veteran and founder of The FerryBridge Group, a consulting agency that specializes in naval and national security issues.
"I watched enough of my friends have issues like this and be removed from command," he added.
Tuesday's incident also raises questions about how a foreign vessel was able to come so close to a US Navy ship operating in a region experiencing heightened tensions between the US and North Korea.
President Donald Trump declared he would be prepared to act "unilaterally" against Pyongyang in early April.
And the arrival late last month of the Vinson strike group, which also includes guided-missile destroyers USS Wayne E. Meyer and USS Michael Murphy, was described as a show of force in advance of a long-anticipated sixth nuclear test from the North Korean government.