[10] The Northern Railroad was incorporated on March 23, 1881, and it planned to build a road from Astoria to Northport via Flushing, Great Neck, Glen Cove, Oyster Bay and Huntington.

[10] By June 1881, construction plans were authorized and in mid-July the building contract was signed, with work set to begin in August.

[10] The Long Island Rail Road attempted to undermine the Northern Railroad's project before it could sell stock and acquire a roadbed.

[10] In February 1883, Austin Corbin, president of the Long Island Rail Road, offered to supply iron and rolling stock for the extension to Oyster Bay if local residents provided the right-of-way.

[10] On Tuesday, June 25, the extension opened for regular passenger service with eight round trips daily to and from Long Island City.

[10][9]: 8 The line ended at Locust Valley for two decades until a final extension added four miles (6.4 kilometers) to Oyster Bay.

In 2009, the LIRR replaced the bridge over West Shore Road between Locust Valley and Oyster Bay Stations.

[21] In the late 2010s, the LIRR replaced and raised the bridge over Buckram Road between Locust Valley and Oyster Bay Stations.

In April 2021, then-President Phillip Eng announced that the LIRR entered into an agreement with Alstom to test battery-powered train cars along the Oyster Bay Branch.

[23] West of Mineola, most trains originate or terminate at Jamaica, with some rush hour trips ending at Hunterspoint Avenue, Long Island City, or Penn Station.

Additionally, some rush hour trains express through Mineola in order to prevent congestion on track 3 of the Main Line.