Prospect Expressway, Caton Avenue, Linden Boulevard, Conduit Boulevard, North Conduit Avenue, South Conduit Avenue, Sunrise Highway, North Road, Flying Point Road, Montauk Highway

Direction: East/West
Western Terminus: Brooklyn-Queens Expressway (I-278) in Brooklyn
Eastern Terminus: Montauk Point Lighthouse
Distance: 122.28 miles
Counties: Kings, Queens, Nassau, Suffolk
Signed: Yes

The first section of NY 27 is the Prospect Expressway, a very short expressway that begins at the Brooklyn-Queens Expressway (I-278) and runs to the southeast for a few miles. The Prospect Expressway ends at Church Avenue and Ocean Parkway, and NY 27 is routed through Brooklyn along Caton Avenue and Linden Boulevard. (There is no exit for Caton Avenue from the Prospect Expressway, so it is necessary to use an indirect connection to stay on NY 27 at this point. Eastbound traffic is routed along East 5 Street. Westbound traffic is routed along Coney Island Avenue and Church Avenue. Eastbound truck traffic is routed along 10 Avenue and McDonald Avenue.) Linden Boulevard ends at Conduit Boulevard, which was built to be part of Robert Moses's Cross Brooklyn Expressway (I-878), which was never constructed. NY 27 is routed along Conduit Boulevard to the Belt Parkway. It is then routed along North Conduit Avenue and South Conduit Avenue, the service roads of the Belt Parkway.

Just west of the Queens-Nassau border, North Conduit Avenue and South Conduit Avenue leave the Belt Parkway and come together to form Sunrise Highway. Sunrise Highway is a large divided road with traffic lights. It runs along the south shore, parallel to Merrick Road, through all of Nassau and the western part of Suffolk. In West Babylon, Sunrise Highway becomes an expressway. Sunrise Highway the expressway runs along the south shore until the beginning of the South Fork. In Shinnecock Hills, Sunrise Highway ends and NY 27 is multiplexed with North Road (CR 39). NY 27 is multiplexed with North Road (CR 39) and Flying Point Road (CR 39A) through Southampton, until the end of CR 39A at Montauk Highway. Montauk Highway is a two-lane road with traffic lights. NY 27 is routed along Montauk Highway from CR 39A to Montauk Point, the easternmost point on Long Island. It ends at the Montauk Point Lighthouse. Over 120 miles long, NY 27 is the longest route on Long Island.