The Interborough Rapid Transit Company (IRT), a private operator, had constructed the section of the line from Flushing, Queens, to Times Square, Manhattan between 1915 and 1928.

The Flushing Line has various styles of architecture, which range from steel girder elevated structures to European-style concrete viaducts.

It heads into the west end of Amtrak's Sunnyside Yard, and passes through two underground stations before entering Manhattan via the Steinway Tunnel under the East River.

[11] The IRT Flushing Line's 7 service has the distinction of running trains with the largest number of cars in the New York City Subway.

On July 22, 1887, Walter S. Gurnee and Malcolm W. Niven founded the New York and Long Island Railroad Company (NY&LIRR).

The Dual Contracts were formalized in March 1913, specifying new lines or expansions to be built by the IRT and the Brooklyn Rapid Transit Company (BRT).

[36][37] The line to Main Street had been practically completed at this point, but had to be rebuilt in part due to the sinking of the foundations of the structure in the vicinity of Flushing Creek.

[43] In July 1920, the New York State Public Service Commission announced it would extend the Flushing Line two stops west to Times Square, with an intermediate station under Bryant Park.

Since work on the project had to be completed underneath the foundations of several large buildings, such as theatres, and the north end of the New York Public Library, the contractor had to provide a $1 million bond.

[48] The project was expected to reduce crowding on the 42nd Street Shuttle by enabling riders to use the Queensboro Subway to directly access Times Square.

[54] Local civic groups advocated for the Fifth Avenue station to be used as a temporary terminal while the permanent terminus at Times Square was being completed.

[64] On February 8, 1927, the New York City Board of Transportation informed the New York State Transit Commission that work on the Times Square station was sufficiently completed to enable the start of train service beginning on February 19, 1927 with the completion of work to a point between Eighth Avenue and Seventh Avenue.

[70] Currently and historically, the IRT assigned the number 7 to its Flushing Line subway service, though this did not appear on any equipment until the introduction of the R12 rolling stock in 1948.

In January 1913, groups representing communities in south Flushing collaborated to push for an elevated along what was then the LIRR's Central Branch,[72]: 53–55  in the current right-of-way of Kissena Corridor Park.

[72]: 277  Shortly after, the New York Public Service Commission (PSC) announced its intent to extend the line as an el from Corona to Flushing, with a possible further extension to Little Neck Bay in Bayside.

[72]: 56  There was consensus that the line should not abruptly end in Corona, but even with the 5.5-mile-long (8.9 km) extension to Bayside, the borough would still have fewer Dual Contracts route mileage than either Brooklyn or the Bronx.

[72]: 61  Under the revised subway expansion plan put forth in December 1913, the Flushing Line would be extended past Main Street, along and/or parallel to the right-of-way of the nearby Port Washington Branch of the LIRR towards Bell Boulevard in Bayside.

The LIRR moved to block the IRT extension past Flushing since it would compete with the Port Washington Branch service in Bayside.

[72]: 62  One member of the United Civic Association submitted a proposal to the LIRR to let the IRT use the Port Washington Branch to serve Flushing and Bayside, using a connection between the two lines in Corona.

[72]: 63 [76] The LIRR president at the time, Ralph Peters, offered to lease the Port Washington and Whitestone Branches to the IRT for rapid transit use for $250,000 annually (equivalent to $7,530,000 in 2023), excluding other maintenance costs.

The Flushing Business Men's Association kept advocating for the Amity Street subway, causing a schism between them and the rest of the groups that supported the LIRR lease.

[78][72]: 67  The Third Ward Rapid Transit Association wrote a report showing how much they had petitioned for Flushing subway extensions to that point, compared to how little progress they had made in doing so.

[72]: 72  As part of the 1929 IND Second System plan, the Flushing Line would have had branches to College Point and Bayside east of Main Street.

[90][91] IDENTRA used a removable round circular disc type radio antenna assembly, slide-mounted on the small mounting brackets that were attached on the front of R12, R14, R15, and R17 cars that were assigned to the 7 route, which had been used on the line since 1948.

Similar to the use of radio transponders in the CBTC installation, the system used the antennas to determine whether a train was running local or express, and then accordingly switched the track at interlockings near the Queensboro Plaza and Flushing–Main Street stations.

Some columns that supported elevated structures on the Flushing Line were so shaky that trains did not run when the wind speed exceeded 65 miles per hour (105 km/h).

The MTA advertised this change by putting leaflets in the New York Times, the Staten Island Advance, the Daily News, and Newsday.

The $70 million rehabilitation project on the Queens Boulevard concrete viaduct was completed six months early, and <7> express service was restored on August 21, 1989, without stopping at 61st Street–Woodside.

[107] In January 2012, the MTA selected Thales for a $343 million contract to set up a communications-based train control (CBTC) system as part of the plan to automate the line.

[113] The whole line was cutover to CBTC operation on November 26, 2018, with the completion of the segment from Hudson Yards to the north of Grand Central.