Objective: A rosette-forming glioneuronal tumor (RGNT) is a rare entity originally described in the fourth ventricle. Recently, RGNTs occurring in extraventricular sites and those with malignant behaviors have been reported. The purpose of this study was to analyze the clinicoradiological and histopathological features, therapeutic strategies, and outcomes of RGNTs. Methods: We enrolled 38 patients diagnosed with RGNTs pathologically between August 2009 and June 2016. CT and MRI, including diffusion-weighted imaging and spectroscopy, were performed. The surgical treatment and histopathological and molecular features were assessed. Additionally, we searched the relevant literatures and performed a pooled analysis of individual patient data. The potential risk factors of prognosis were analyzed. Results: Our case series included 22 male and 16 female patients, with a mean age of 25.9 years. RGNTs involved the fourth ventricle (26.3%), cerebella (34.2%), supratentorial ventricular system (13.2%), spinal cord (10.5%), temporal lobe (10.5%), thalamus (7.9%), brain stem (7.9%), frontal lobe (5.3%), pineal region (5.3%), suprasellar region (2.6%), and basal ganglia (2.6%). Statistical analyses showed that pediatric age, purely solid appearance of the tumor, and inadequate resection (only partial removal or biopsy) were risk factors associated with progression events. Patients with subtotal resection appeared to do as well as those with gross total resection. Conclusions: RGNTs can occur nearly anywhere in the CNS, at both supratentorial and infratentorial sites. Maximal safe surgical resection should be emphasized for treatment; whilst aggressive resection with the goal of complete resection may be unnecessary.