Gliomas are the most common and aggressive primary tumours of the central nervous system in adults. Bone marrow-derived mesenchymal stem cells (BMSCs) are an important component of the glioma microenvironment. Our previous study indicated that BMSCs in the glioma microenvironment could be induced to malignantly transform by glioma stem cells (GSCs). The malignant transformation of BMSCs is closely related to glioma progression; however, the underlying mechanism of this transformation has not been fully clarified. In this study, we found that compared with the levels in normal BMSCs, the levels of the long noncoding RNA FTX transcript XIST regulator (lncRNA-FTX) were increased in malignantly transformed BMSCs (tBMSCs), which was associated with the proliferation, migration and invasion of tBMSCs. Next, by using a luciferase reporter assay and an RNA pull-down assay, we found that lncRNA-FTX acted as a sponge for miR-186 in tBMSCs. Further research revealed that miR-186 could bind to the 3ʹ-UTR (untranslated region) of c-Met, which acts as an oncogene in gliomas. Through functional assays, we showed that lncRNA-FTX could regulate c-Met expression in tBMSCs in a miR-186-dependent manner. Based on these data, we concluded that lncRNA-FTX plays a key role in the GSC-mediated malignant transformation of BMSCs in the glioma microenvironment, which is of great significance for further understanding the pathogenesis of glioma.