Originally an Interborough Rapid Transit Company-operated route, it was built as part of the Dual Contracts expansion and opened in 1917 and 1918.

The Woodlawn Line also has a connection to the Jerome Yard, where 4 trains are stored, just north of the Bedford Park Boulevard–Lehman College station.

[3] Though named for Jerome Avenue, the southernmost portion of the line runs underground beneath the Grand Concourse.

After the northwest entrance of the historic Concourse Yard and then north of 198th Street, the road briefly moves east of the line.

When the first subway was being planned, a branch of the line to this area was under consideration, but it was not found to be feasible to build such a connection because of financial reasons.

Route 16 called for a three-track elevated line along Jerome Avenue, extending from Clarke Place north to Woodlawn Road.

Of the three options, Route 15 was approved by the New York City Board of Estimate on July 14, 1905, and by Mayor George McClellan two weeks later.

A paper transfer issuance was established between the shuttle and the IND Concourse Line station at 155th Street at the Polo Grounds.

[14] Dual third rail operation remained in use on the Jerome Avenue Line to the yards at Bedford Park until shuttle service ended in 1958; the structure and the bridge were removed in 1962.

[19][14][20] In Fiscal Year 1960, work began on the extension of platforms at some stations on the line to 525 feet (160 m) to accommodate ten-car trains.

[21] In 1986, the New York City Transit Authority launched a study to determine whether to close 79 stations on 11 routes, including the Jerome Avenue Line north of 167th Street, due to low ridership and high repair costs.

As part of the project, new canopy roofs, walls, lighting, staircases, floors, token booths, and public address systems would be installed at each station.

As part of the project, station mezzanines were refurbished, electrical upgrades were completed, platform floors, canopy roofs, and windscreens were replaced.

[30] From October 26, 2009, to December 11, 2009, another pilot program to run express service ran, this time adding Bedford Park Boulevard–Lehman College as an additional stop.