The Rockefeller Center station was built for the Independent Subway System (IND), which had first proposed constructing a line under Sixth Avenue in 1924.

[5] In 1924, the IND submitted its list of proposed subway routes to the New York City Board of Transportation (BOT), which approved the program.

[9] The IND started advertising bids for the section of the Sixth Avenue Line between 43rd and 53rd Streets in April 1931.

[10] In April 1935, engineers started planning in earnest for the Midtown portion of the Sixth Avenue Line.

[11] The city government issued corporate stock to pay for the $53 million cost of the project, since the line was not eligible for federal Public Works Administration funds.

[12][13] The first contract, for the section between 40th and 47th Streets (just south of the Rockefeller Center station), was awarded to Rosoff-Brader Construction in October 1935.

[14][15] Mayor Fiorello H. La Guardia broke ground for the Sixth Avenue subway at Bryant Park on March 23, 1936.

The work largely involved cut-and-cover excavations, although portions of the subway had to be tunneled through solid rock.

[20][23] Workers used small charges of dynamite to avoid damaging nearby buildings or the Catskill Aqueduct, which ran below Sixth Avenue and was a major part of the New York City water supply system.

[20] By the beginning of the following year, the track junction north of the station was being constructed at a rate of 5 feet (1.5 m) per day.

[26] The bellmouths diverged from the local and express tracks on both the northbound and southbound sides of the station, with tunnels that stub-ended at 53rd Street.

[27] The station opened on December 15, 1940, as part of the mainline portion of the IND Sixth Avenue Line to West Fourth Street–Washington Square.

[31] The BB train served part of the Sixth Avenue Line's midtown section during weekday rush hours only, running local between 168th Street and 34th Street–Herald Square.

[32][33] In early 1949, the BOT announced that an automatic shoe-shine machine would be installed at the station as part of a pilot program.

[34] To improve cleanliness, the BOT also installed a "hygiaphone" at the station agent's booth; the device was composed of a transparent membrane and was meant to reduce the spread of germs.

[37] In February 1958, Rockefeller Center Inc. leased 15,000 square feet (1,400 m2) in the northern mezzanine for 20 years at a total cost of $2 million over that period.

Architects Harrison & Abramovitz were hired to redesign the mezzanine with stores similar to Rockefeller Center's underground mall.

[46] The NYCTA installed turnstiles and stairways to accommodate the additional passenger traffic, and Rockefeller Center Inc. paid for the improvements.

In addition, Rockefeller Center Inc. built a passageway between 47th and 49th Streets, running parallel to the station's mezzanine.

[50] In 1994, amid a funding shortfall, the administration of mayor Rudy Giuliani proposed delaying the station's renovation.

[55] The MTA again proposed renovating the station as part of its 2005–2009 capital program, but it postponed these plans in 2005 due to a lack of funding.

[59]: 125  Rockefeller Center's underground mall, built in 1935 as part of the complex's construction,[67] contains passageways to the station's mezzanine.