The slow-motion stampede began about 6:45 a.m. (1045 GMT), and within three hours there were so many turtles on Runway 4L 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 US Department of Agriculture were scooping up turtles and moving them across the airport, he said. Flight delays averaged about 30 minutes, the FAA said.
The migration of diamondback terrapin turtles happens every year at John F. Kennedy International Airport, which is built on the edge of Jamaica Bay and a federally protected park. In late June or early July the animals 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 Runway 4L just as the morning rush hour was beginning at JFK, according to a radio recording posted on LiveATC.net.
"Be advised 30 feet (10 meters) 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 as the big airliner climbed into the air.
American 663, a Boeing 737 headed to Fort Lauderdale, found its way to runway 4L blocked by three of the roving reptiles. After ground crews removed them, the plane taxied into takeoff position, received takeoff clearance - and was promptly blocked by more turtles.
American and JetBlue, which has a hub at JFK, both said there were no major disruptions to their flights.
"We hope for faster animals next time," JetBlue said in a statement.
Diamondback terrapins can grow up to 9 inches (23 centimeters) long and weigh up to 3 pounds (1.4 kilograms), but most average about half that size.
Wayward wildlife is a serious concern at JFK and nearby LaGuardia Airport, which both sit on shorelines populated by geese, turtles, ducks, frogs and other animals.
In January 2009 a US Airways plane bound for Charlotte, N.C. was forced to land in the Hudson River after it hit a flock of birds and lost power in both engines. All 155 passengers and crew members were rescued.
In the past year, 101 planes have been damaged by bird strikes at JFK, two of them badly, according to a database kept by the FAA.
The main concern is for the turtles themselves, Marsico said. He said crews were loading the turtles into pickup trucks and giving them rides to the nesting beaches.