Littleton-Downtown station's depot opened on January 1, 1872 as a flag stop on the Denver & Rio Grande Railroad's Royal Gorge Route.

Between the Denver & Rio Grande Railroad, and the adjacent Denver, South Park and Pacific Railroad and Atchison, Topeka and Santa Fe Railway, downtown Littleton saw 24 daily intercity passenger trains at its peak.

[11] In 2022, Nook Coffee began using the building with support from Littleton's City Council, but shut down in March 2024.

The station platform is located in the open cut Colorado Joint Line, necessitating the use of stairs or a ramp to access it.

[16][17] Littleton-Downtown station is located on the western edge of Downtown Littleton, with the Sterne park neighborhood directly to the south and east.

[18] The Littleton Main Street Historic District is kitty-corner to the station's northwest, which also includes the Town Hall Arts Center.

The furthest development from the station itself, roughly half a mile away, is the Nevada Place condominiums, which consist of 31 strictly residential units.

Littleton-Downtown station is served by the D Line, which runs from Littleton to Downtown Denver via Sheridan, Englewood, Overland, Baker, Lincoln Park, and Auraria.

[23] D Line trains serve Littleton-Downtown station from 4:00 a.m. to 12:30 a.m. Monday through Thursday, however service lasts until 1:00 a.m. on Sundays and holidays, and until 2:00 a.m. on Fridays and Saturdays.

During most hours of the day, the D line serves Littleton-Downtown station every 15 minutes, however headways become longer early in the morning and late at night.

The painting was inspired by the Robert McQuarie book Settlement to Centennial as well as photos from the Littleton Historical Museum.