Construction of the second section of the railway continued in 1885 and 1886 to large settlements of Turkmenistan: Geok Tepe, Ashgabat, Tejen, Mary, and Chardzhou (today's Türkmenabat, ending at the Amu Darya.

[2] In 1922, on the instructions of Vladimir Lenin, work began on the design of Soviet diesel locomotives for operation on waterless sections of Central Asia.

During the battles near Stalingrad and the Caucasus (from August 1942 to February 1943), the Krasnovodsk port and Ashgabat railway station became the only transport arteries connecting Baku, Transcaucasia and the Black Sea with the whole country.

After the collapse of the USSR, the construction of new lines again intensified, forced by the fact that the previous routes were interrupted by sections that became part of the Uzbek railways and therefore crossed international boundaries.

During the period after the collapse of the USSR, a number of new trunk lines were opened in Turkmenistan: Takhiatash (Uzbekistan)-Kunya-Urgench-Saparmyrat Türkmenbaşy adyndaky, Türkmenabat-Kerki-Kerkiçi, Tejen-Sarakhs (Iran), Ashgabat-Daşoguz, which made it possible to connect disparate sections of the railway network into a unified whole.

On March 3, 1992, the "Great President of Turkmenistan" Saparmurad Niyazov approved the Regulation "On the Turkmen Railway", according to which the Turkmen Railway was defined as a legal entity, a single production and economic complex operating on the principles of full-cost accounting and self-financing, combining economic management methods with centralized management of the transportation process.

[5] In 1996, the Mashhad–Sarakhs extension connected Iran to Turkmenistan, as part of the Silk Road railway for linking the landlocked Central Asian countries to the Persian Gulf.

[11][12] Another rail line was opened farther east in November 2016, connecting Aqina in Faryab province via Ymamnazar with Kerki in Turkmenistan.

[14] It is planned to become part of a rail corridor through northern Afghanistan, connecting it via Sheberghan to Mazar-i Sharif and on to the border with Tajikistan,[15] although it is unclear when this will happen.