The sole line started from Segner square, crossed the tram line at the Great Railway Station (Nagyállomás), and traveled on the northeastern main road of the city reaching the site of the Hungarian Roll Bearing Industries (Magyar Gördülőcsapágy Művek, MGM).

After a year in service in 1986, the network expanded two stops from the MGM to the main gate of the Public Cemetery (Köztemető), and a year later with line number 3, that shared the exact same end stations as its original counterpart, but instead of the outer ring of the city, the line crossed through the inner city to reach its destination.

Although pole-laying operations started at Tócóskert as well, the quickly draining financial situation of the city made the construction works impossible to finish.

In 2000, the line 4A was suspended in favor of bus operator Hajdú Volán's new methane fueled green buses, and traffic on it was restored in 2010 only (as line number 4), a year after Hajdú Volán lost its position as Debrecen's local bus operator.

In 2005, the city of Debrecen bought new Ganz-Solaris Trollino 12 trolleybuses, with 5 of them (later expanded to 16) being capable of moving without cables as diesel powering was fitted in them.