Glioma is the most common and fatal tumor of the central nervous system in humans. Despite advances in surgery, radiotherapy, and chemotherapeutic agents, glioma still has a poor prognosis. The tumor microenvironment (TME) of glioma is of highly complex heterogeneity, which relies on a network-based communication between glioma cells and other stromal cell types. Exosomes are the most common type of naturally occurring extracellular vesicles, ranging in size from 40 to 160 nm, and can serve as carriers for proteins, RNAs, and other biologically active molecules. Recent evidence has shown that glioma-derived exosomes (GDEs) can be integrally detected in the local tissue and circulatory blood samples, and also can be transferred to recipient cells to mediate transmission of genetic information. Non-coding RNAs (ncRNAs) mainly including microRNA, long non-coding RNA, and circular RNA, account for a large portion of the human transcriptome. A broad range of ncRNAs encapsulated in GDEs is reported to exert regulatory functions in various pathophysiological processes of glioma. Herein, this review summarizes the latest findings on the fundamental roles of GDE ncRNAs that have been implicated in glioma behaviors, immunological regulation, diagnosis potential, and treatment resistance, as well as the current limitations and perspectives. Undoubtedly, a thorough understanding of this area will provide comprehensive insights into GDE-based clinical applications for combating gliomas.