The turtles were crossing Runway 4L, apparently to reach sand along the other side of the runway, that juts out into the water.
Port Authority workers picked up the turtles and moved them to the sand.
The turtles, classified as Diamondback Terrapins, started meandering across the runway about two weeks ago. They are expected to continue visiting the runway through July.
Jets hit turtles a few times each year at Kennedy Airport, usually in the final days of June or earliest days in July, according to the FAA's wildlife strike database.
Wednesday's slow-motion stampede began about 6:45 a.m., and within three hours there were so many turtles on one runway and nearby taxiways that controllers were forced to move departing flights to another runway.
"We ceded to Mother Nature," said Ron Marsico, a spokesman for the Port Authority of New York and New Jersey, which owns the airport.
Workers from the Port Authority and the U.S. Department of Agriculture were scooping up turtles and moving them across the airport, he said. Flight delays were averaging about 30 minutes, the FAA said.
The migration happens every year at Kennedy, which is built on the edge of Jamaica Bay and a federally protected park. In late June or early July, they heave themselves out of the bay and head toward a beach to lay their eggs.
The peak of the migration usually lasts a few days, Marsico said.
Several pilots, some of them stifling chuckles, began reporting turtles on the runway just as the morning rush hour was beginning at JFK, according to a radio recording posted on LiveATC.net, which streams and records air traffic radio feeds.
"Be advised 30 feet into the takeoff roll, left side of the centerline, there's another turtle," called the pilot of American Airlines Flight 1009, a Boeing 767 that had just taken off bound for the Dominican Republic.
"There's another one on the runway?" asked the controller.
"Uh, well he WAS there," the pilot said with a laugh.
American 663, a Boeing 737 headed to Fort Lauderdale, found its way to runway 4L blocked by three of the roving reptiles.