Part of the New York City Subway, it split from the IND Queens Boulevard Line at an existing flying junction east of Forest Hills–71st Avenue station, ran through the Jamaica Yard and then ran northeast and north through Flushing Meadows–Corona Park, roughly along the current path of the Van Wyck Expressway.

The line continued along a wooden trestle to the World's Fair Railroad Station, located slightly south of Horace Harding Boulevard (now the Long Island Expressway).

[7] At the time, the Queens Boulevard Line of the city-operated Independent Subway System (IND) was being extended to Union Turnpike, and the Jamaica Yard was being built in Flushing Meadows as a storage depot for trains.

[18][19] According to Whalen, without the spur, 70% of the fair's visitors would be forced to use the BMT and IRT station at the extreme north end of the fairground,[18] and IND riders would be disadvantaged because they would have to pay an additional 10 cents to transfer to a bus.

[20] Conversely, Moses derided the line as "extravagant and unnecessary",[21][22][23] prompting Mayor Fiorello La Guardia to convene a committee to discuss the spur's construction.

[24] Despite Moses's objections, the Board of Estimate approved $1.2 million for the World's Fair spur that March.

[25][26] New York state lawmakers John J. Dunnigan and Herbert Brownell Jr. sponsored legislation in April 1937 to authorize the Board of Estimate to issue $1.2 million worth of bonds for the project.

[35][36] For legal and financial reasons, the line was called the "World's Fair Railroad" and was considered a separate entity from the IND, in part due to the state legislation.

[39][40] The plans for the IND World's Fair Line prompted increased interest in homes that were being built near the spur.

They also looked at the possibility of intermediate stations along the line to serve the local areas, comprising what is now Kew Gardens Hills and Flushing.

[44] Attractions in Flushing Meadows, such as the Citi Field baseball park and the USTA National Tennis Center, were not added until later.

[45] La Guardia sent an emergency message to the Board of Estimate in September 1937, requesting funding for the spur.

The company had been the lowest bidder for the contract, having offered to construct the trestle for the World's Fair Line at a cost of $308,770.

[48][49] As part of the contract, the Cox Company was to construct a pile trestle along the eastern edge of Flushing Meadows, with track beds made of rock ballast.

[51] The same month, the Board of Estimate awarded nine contracts for the construction of the line's tracks, which cost a total of $148,595.

The turnstiles were configured to accept either nickels or dimes because the BOT had not yet decided whether to implement the increased fares.

[59][60] To pay for the line's construction, the Board of Estimate decided in February 1939 to charge an additional fare at the World's Fair station.

[2]: 314, 409 [3]: 83 [69] The line was mostly served by the GG local train, running between Smith–Ninth Streets and the World's Fair station.

[61] Additional E express service ran between the World's Fair station and Hudson Terminal during afternoon rush hours and evenings.

[73] Reflecting the IND line's temporary nature, it had to be repaired and reinforced every time there was a severe rainstorm.

[78]: 189 [76][77] The IND World's Fair Line was closed between seasons,[3]: 27, 83 [79] and police officers patrolled the area outside the station during the off-season.

[80][81] That June, Harvey proposed retaining the line after the fair,[82][83] and he formed a committee to advocate for its continued operation.

[45] The right-of-way was replaced with an extension of 136th Street, and eventually the northern portion of the Van Wyck Expressway which formed today's Interstate 678.

Moses, who was also in charge of the corporation that operated the 1964 fair, rejected the proposal once he found out that the line would have cost $10 million.

[58] The closest attractions to the station were the New York State Amphitheater (also known as the Aquacade) and the World's Fair Music Hall.

[95] Before the beginning of the 1940 season, thirty lights were installed on the ramp leading to the World's Fair station.

Due to the expense of removing the pilings, workers decided to leave the foundations in place after the fair.