The line was inaugurated on 12 July 1915. It was partially destroyed during World War II, and gradually reopened between October 1944 and May 1953. Passenger numbers peaked at 3,001,900 in 1975. In the late 1970s, due to its poor financial results and the risk of closure, the railway was taken over by the Province of Perugia. In 2000, the rail operator was reorganized into a company owned by the regional government, and in December 2010 it was subsumed into a holding company gathering all the regional public transport services. In 2009, the company employed 211 people. In the late 2000s, the company depended on public subsidies for 71% to 87% of its operating income. In December 2005, a service linking Sansepolcro to Roma Termini station was launched. In April 2013 a train came off the rails near Umbertide, injuring 23 passengers. The regional public transport holding, Umbria Mobilità, was sold to Busitalia in 2014. All passenger services were cancelled in September 2017 and partially restored in October 2018; they now operate on a section between Città di Castello and Perugia Ponte San Giovanni.
Infrastructure
The main line has a maximum grade of 2%, reaching 6% on the branch between Perugia Sant'Anna and Perugia Ponte San Giovanni. The minimum curve radius is on the main line, and between Perugia Sant'Anna and Perugia Ponte San Giovanni. The speed limit on the line was originally set at, with an average travel speed of. Due to the poor state of maintenance of the tracks and regulatory changes after the Andria–Corato train collision in 2016, the limit was lowered to in October 2016, and further reduced to a maximum speed of in October 2018. Stations north of Perugia, such as the ones in Umbertide and Città di Castello, tend to be close to the city center, while south of Perugia they are generally more remote.
Passenger services
According to a 2013 survey, 25.9% of trains ran with fewer than 30 people on board, reaching 71.6% between Sansepolcro and Città di Castello. The busiest segment is the line between Ponte San Giovanni and Perugia Sant'Anna with an average of 2,400 passengers per day. Several stations and stops recorded an average of zero passengers per day.
Rolling stock
As of 2014 the rolling stock was made up of 45 diesel-powered ALn 776 and four electric-powered Minuetto trains. The ALn 776 trains were built between 1986 and 1993. The four Minuettos were purchased in 2008. Owing to the high cost of spare parts, as of 2014 three are nonoperational, while one remains in active service.
Routes
The following stations, stops and halts were served in December 2010, many of them as request stops. As of May 2019, most are inactive; stations currently served by rail are marked with a green diamond. Route Terni – Todi – Ponte San Giovanni – Perugia Sant'Anna:
