Alterations of N6-methyladenosine (m6A) RNA modifications are responsible for a platter of structural and functional changes in healthy and cancerous cell states. Even though several studies have linked m6A to the onset and development of tumors, very few have examined transcriptome-wide m6A landscape of long non-coding RNAs (lncRNAs) in cancerous cells, including gliomas. This work aims to explore and elucidate lncRNA m6A alterations and expression in glioma stem cells, U87-MG cells and glioma patients. We utilized four cell lines (NCH421k, NCH644, NCH690, U-87 MG), along with 16 glioblastomas (GB) and 9 low grade (LGG) gliomas. m6A RNA modifications were detected using MeRIP-seq and dRNA-seq. First, we provided transcriptome-wide lncRNAs m6A peak distribution in GSCs. MERIP-seq analysis between U-87 MG and GSCs showed 76.4% overlap of lncRNAs m6A peaks, while 19.4% of peaks were exclusively identified in GSCs. Next, m6A was observed uniquely in GSCs for previously identified glioma-associated lncRNAs, including LINC000461, HOTTIP, CRNDE, TUG1, and XIST. Further, dRNA-seq transcript hierarchical clustering analysis revealed differentially expressed lncRNAs capable to separate LGG, GB, and GSCs (NEAT1, ANAPC1P2, CYTOR, ZNF8-ERVK3-1, MIR4435-2HG, LINC01116, and MIR222HG). Subsequently, PCA analysis based on lncRNA expression pattern identified clusters attributed to GSCs-GB and LGG. Additionally, we discovered that a set of lncRNAs were associated with stemness transcript activation in gliomas and worse patient survival (p<0.05). Our findings offer a foundation and understanding for further research on m6A modifications and expression patterns in the non-coding epitranscriptome of GSCs and glioma.