The town of Schleusingen includes next to the core town another seventeen districts: Altendambach, Breitenbach, Erlau, Fischbach, Geisenhöhn, Gethles, Gottfriedsberg, Heckengereuth, Hirschbach, Hinternah, Oberrod, Rappelsdorf, Ratscher, Schleusingerneundorf, Silbach, Sankt Kilian and Waldau In addition, terms for residential areas such as' 'Upper-' 'and' 'Lower Town, Schmuckplatz, Weißer Berg, Hirtengrund, Kalkrangen, Sonneneck, Rubetal ' etc.
Count Poppo VII of Henneberg built the Bertholdsburg as a residence and fortification in the period from 1226 to 1232.
In 1412 Schleusingen received the Stadtrecht (the right to be considered a town) but only in 1533 the Marktrecht [de] (the right to, among other things, hold a folk festival or a weekly market).
During the riots in the German Peasants' War in the spring of 1525, the inhabitants, documents and valuables of the neighboring monasteries Veßra and Trostadt [de] were sent to Schleusingen to be brought to safety at the Bertholdsburg.
The Aegidienkapelle of the St. Johannis Church became the burial place of the Counts of Henneberg in 1566 and of Elisabeth of Brandenburg.