RFTA's service area stretches 70 miles (110 km) from Aspen to Rifle, serving the towns in between consisting of Basalt, Snowmass Village, Carbondale, Glenwood Springs, New Castle, and Silt.

[4] Transportation in the Roaring Fork Valley dates back to the late-1880s, when the Denver and Rio Grande Railroad ran their first train to Glenwood Springs on October 5, 1887.

Denver and Rio Grande's competitor, Colorado Midland Railway, reached Aspen the same year, and completed their connection downvalley to Glenwood Springs on December 9, 1887.

Also during this time period, the Environmental Protection Agency designated Aspen as a PM10 non-attainment area, resulting in RFTA increasing services to reduce air pollution and vehicle miles traveled, particularly along the SH 82 corridor.

[11][4][10] In 1994 the Roaring Fork Railroad Holding Authority (RFRHA) was created as a public entity to purchase the former Denver and Rio Grande Aspen Branch between Glenwood Springs and Woody Creek.

The corridor was converted to a rail trail and railbanked for a future mass transit line to reduce congestion on SH 82.

[4][10] Service was temporarily extended to Parachute during a 95-day replacement of the Grand Avenue bridge in Glenwood Springs from August 14 to November 22, 2017.

[17] In September 2020, Parachute Area Transit System (PATS) began service to Battlement Mesa and Rifle, connecting with RFTA at the latter.

Twenty-two compressed natural gas (CNG) buses with free on-board Wi-Fi were introduced with the VelociRFTA bus rapid transit line.

[26] RFTA's system offers express service throughout the Roaring Fork Valley from Glenwood Springs to Aspen since September 3, 2013.

[27] To promote the new service, RFTA placed giant concrete and foam eggs at selected bus stops, and cast dinosaur footprints in nearby sidewalks.