The station first opened in a local store as Waverly around 1843. Although the surrounding area was renamed Holtsville in 1860 when a post office opened, the station retained the name "Waverly" until the 1890s, when farmers complained about their shipments going to an upstate town named Waverly by mistake. Holtsville Station was rebuilt on May 13, 1912, only to be burned in another fire on January 4, 1914, and replaced again later the same year South of the station was the northern terminus of the Suffolk Traction Company's main trolley line, which was proposed to be extended to Port Jefferson, New York, across a bridge over the tracks before the company went bankrupt in 1919. The station buulding was bulldozed in June 1962, but the station itself continued to operate until March 16, 1998, when it was closed along with several others due to low usage, which didn't make it very cost effective to install high-level platforms needed to support the then-new C3 bi-level coaches.
^Bayles, Richard Mather. Bayles' Long Island Handbook (Budget Steam Print: Babylon, New York, 1885) (1885 guidebook notes that the train station is called Waverly)
^"Holtsville History Recalled as a Result of Handbook Story". Mid-Island Mail. November 13, 1935.|accessdate= requires |url= (help)("According to the Terrys and Mr. Bates the name was changed in 1897, on petition of the residents, mostly farmers, of Selden and Farmingville.")
^"The Long Island Rail Road in Early Photographs," by Ron Zeil(1990)