The main runway at New York’s John F. Kennedy International will be closed for four months starting today. Millions of travelers will experience delays — including some not flying anywhere near the Big Apple.

With about one-third of JFK’s traffic and half of its departures being diverted to three smaller runways, planes will wait on longer lines on the ground for takeoffs and in the air for landings. Delays at one of the nation’s largest airports will ripple to cities across the U.S., including Los Angeles, San Francisco and Orlando.

Passengers using JFK also face another headache — higher ticket prices. JetBlue, American, Delta and other airlines have cut their schedules by about 10 percent for the shutdown period. They can raise prices because there will be a smaller number of seats to meet demand.

JFK’s Bay Runway, at 14,572 feet, is one of the longest commercial runways in the world. It’s a backup landing spot for the space shuttle, which has its next mission in April. The runway is being repaved with concrete instead of less-durable asphalt and widened to accommodate today’s bigger planes.

The project will affect at least the first month of the peak travel season, which officially starts on Memorial Day. But the chosen four-month period was picked because it’s the driest in the New York area, making weather-related construction delays less likely. Of course, prompt completion isn’t certain. A similar runway repair in Minneapolis last year created thousands of delays when it was slowed by unseasonably wet weather.

JFK is already one of the nation’s most delay-plagued airports. It ranked 28th out of 31 major airports in 2009 in on-time performance, according to the Department of Transportation. A delay at JFK, especially one early in the morning, can push back flights across the U.S.

The longest delays occur at peak hours — from about 8:30 to 9:30 a.m. ET and between 5:30 and 6:30 p.m.

The airlines and the airport are making adjustments. Besides cutting flights, airlines are adding time into their schedules. So although flights may take longer, more won’t necessarily be considered late. Still, Mike Sammartino of the Federal Aviation Administration expects delays at JFK will be about 50 minutes during peak times and 29 minutes on average — similar to busy summer days.

Sammartino also says JFK officials have added new taxi ways at angles that allow planes to go from terminal to takeoff more quickly. He noted that the FAA and the Port Authority of New York and New Jersey, which are financing the $376 million project, began planning the shutdown in early 2009.

JetBlue, the biggest carrier at the airport, said it expects some “operational challenges,” but that its reduced flight schedule should help alleviate congestion.

However, for passengers on network carriers like Delta and American the delays will likely be worse, said Lance Sherry, executive director for the Center for Air Transportation Systems Research at George Mason University. JetBlue already tends to avoid the rush hours at JFK. And it has fewer connecting flights, which push delays across the country.

Even if you avoid big delays, you could face higher fares. George Hobica of Airfarewatchdog.com said some fares are up significantly for the March-June period. For example, the lowest published fares for flights between JFK and Los Angeles International Airport through June 20 range between $278 and $298 roundtrip. That’s up from $198 to $218 recently. Delays and higher fares will affect Los Angeles travelers the most because the city is the most popular domestic destination from JFK, followed by San Francisco and Orlando.

Airfares usually rise as spring approaches. But the lowest published fare from LaGuardia, just 8 miles west of JFK, is $100 cheaper for a connecting flight in the same time period — a more significant gap than normal. Nonstop flights to the West Coast aren’t available from LaGuardia.

The shutdown also affects the coordination of flights, and the people who make sure the planes take off and land safely.

Steve Abraham says he and his fellow JFK air traffic controllers must learn how to move aircraft efficiently without the use of their biggest runway. That could add more time to takeoffs and landing, at least initially. Fifty percent of the controllers at JFK have less than 4 years of experience.

“It’s like renting a car in England — you know how to drive but you’re driving on the other of the road,” Abraham said. “I know how to say ‘clear for take off’ but I’m just doing it in a configuration that I’m not used to.”

JFK airport officials opted for the four-month total shutdown rather than a construction schedule that included overnight work for 2 to 3 years. That’s a move Abraham says air traffic controllers support.

“I’d much rather inconvenience people for four months than for two years.”