Glioblastoma (GBM) is the most common primary malignant intracranial tumor with a very poor prognosis. In this study, we systematically analyzed the DNA methylation alterations of autophagy-related lncRNAs and their association with drug therapies in GBM. We identified 9 DNA methylation-dysregulated lncRNA regulators of autophagy-related genes as autophagy-related lncRNAs. A dysregulated regulatory network consisting of 9 autophagy-related lncRNAs and 237 differentially expressed autophagy-related genes was constructed. Identification of small molecule drug candidates that may affect DNA methylation dysregulated lncRNA activity, including 45 drug lncRNA pairs, involving 7 DNA methylation dysregulated lncRNAs and 43 drugs. Furthermore, we identified a DNA methylation-dysregulated autophagy-related lncRNA MIR155HG as an independent prognostic indicator for GBM. The significantly decreased methylation level of the MIR155HG promoter contributed to its up-regulated expression, which was involved in autophagy regulation through the regulation of autophagy-related genes WMP1, AP4M1, and UBQLN2. Our results showed that DNA methylation-dysregulated lncRNAs may be potential biomarkers and drug targets in GBM through regulating autophagy-related functions.