It branches north from the Main Line at the former Winfield Junction station, just east of the Woodside station in the New York City borough of Queens, and runs roughly parallel to Northern Boulevard past Mets-Willets Point (Citi Field), Flushing, Murray Hill, Broadway, Auburndale, Bayside, Douglaston, Little Neck, and then crosses into Nassau County for stops in Great Neck, Manhasset, and Plandome before terminating at Port Washington.

[6] Extra service is offered during the U.S. Open tennis tournament and for New York Mets home games, both of which are held in Flushing Meadows–Corona Park.

Originally intending to run further east to Roslyn, Oyster Bay, and even Huntington, the NY&F's plans were thwarted by the LIRR who reached those destinations first, as well as poor service and competition with the 1868-established Flushing and North Side Railroad.

In 1869, the New York State Legislature authorized the Flushing and North Side to buy the New York and Flushing east of the LIRR crossing at Winfield Station, while the segment between Hunters Point and Winfield was acquired by the South Side Railroad of Long Island until it was abandoned for passenger service east of what was to become the former Laurel Hill Station in 1875.

[10] Despite a failed attempt to extend the line from Great Neck to Roslyn in 1882, wealthy Port Washington residents persuaded the LIRR to bring the terminus to their hometown in 1895.

The GN&PW was disestablished as a subsidiary in 1902, and that segment simply became part of the Port Washington Branch.

[12] In 1910, the Public Service Commission approved the LIRR's application to eliminate grade crossings along the line.

[20] Alongside this project, a new bridge was built at Colonial Road near Great Neck station; it opened in May 2016 and replaced a 114-year-old span.

[17][26] However, this project met significant community opposition, primarily because of proposed reduction of parking spaces near the station.

[27] As of September 2022[update], the MTA has not come to an agreement with the Town of North Hempstead,[18]: 65  resulting in the project being postponed indefinitely.

At the North Hempstead Town Hall meeting that evening (where the MOU was unanimously approved), Assemblywoman Mariann Dalimonte stated in response to a question from a member of the public that she and Supervisor DeSena had expressed the concern as to whether or not there would be any service improvements from this project to the Metropolitan Transportation Authority, which oversees the LIRR.