Human cases of fatal encephalitis caused by Borna disease virus 1 (BoDV-1) have been increasingly reported. We envisaged the present systematic review in order to provide a comprehensive summary of clinical features associated with BoDV-1 encephalitis. Systematic research of four databases (PubMed, EMBASE, MedRxiv, BioRxiv) was performed during July 2023, and corresponding clinical and epidemiological data were collected and analyzed. A total of 37 BoDV-1 encephalitis cases from 15 different study cases and two countries (Germany, No. 35; France, No. 2) were detected, and their features were summarized (case fatality ratio, 91.9%). Age distribution followed a “U-shaped” distribution, with a first peak in individuals younger than 14 years (18.9%) and the second one in subjects older than 50 years (43.2%). Environmental risk factors were irregularly reported, but 17 out of 37 cases either lived in rural areas or reported repeated outdoor activities (45.9%). Interaction with pets and livestock was reported in eight cases (21.6%), stressing the zoonotic potential of BoDV-1 infections. Moreover, 16.2% of cases were reported among recipients of solid organ transplantations (five kidneys; one liver). Overall survival in children/adolescents vs. adults (≥18 years) was not significantly different (Hazard Ratio 0.878; 95% Confidence Interval from 0.366 to 2.105). Magnetic Resonance Imaging identified the involvement of basal ganglia, mostly of the caudate nucleus (42.4%) and thalamus (33.3%). Cerebrospinal fluid was often characterized by pleocytosis (78.4%). On the other hand, no distinctive clinical features were identified: initial symptoms were specific and included headache, fever, and confusion. In conclusion, BoDV-1 infection can result in fatal encephalitis, whose actual burden still remains unascertained. As the epidemiology of BoDV-1 is similarly elusive, encephalitis cases of unclear cause should be routinely tested for bornaviruses.