Gliomas are the most common primary malignancy that occurs in the adult human brain, with devastating consequences for patients. Within adult diffuse gliomas, there are three subtypes: astrocytoma, oligodendroglioma, collectively termed low-grade glioma (LGG) and glioblastoma (GBM). Despite significant study, many fundamental questions remain including the cell of origin and its functional implications of these cells in disease progression. Oligodendrocyte progenitor cells (OPCs) are the largest pool of proliferation capable cells in the adult brain and give rise to mature oligodendrocytes throughout adult life. We first examined OPCs as a probable cell of origin for IDH1 mutant LGG. In mouse models, we found that OPCs can give rise to LGGs that resemble human tumors. We found that LGGs in our model, arising from both neural stem cells (NSCs) and OPCs, displayed histological, protein, and transcriptomic characteristics reminiscent of GBMs arising from OPCs. Lastly, we found that our mouse models share transcriptomic similarity to human LGGs. Next, we examined the role of OPCs as quiescent cancer stem cells (qCSCs) in GBM. We developed a novel mouse transgene to identify, purify, and ablate OPCs within OPC-driven GBMs in vivo. We show that this transgene can identify functional qCSCs within OPC driven GBMs. Using this transgene and two other methods, we developed three independent gene expression signatures to identify qCSCs within single cell RNA-sequencing datasets. We found that all three of our signatures enrich in a single cluster of putative qCSCs which also had low expression of cell-proliferation related genes. Next, we purified these cells from primary mouse GBMs and showed that they have functional characteristics of qCSCs in vitro. Lastly, we show that these signatures can also identify putative qCSCs within a set of human GBMs. Our collective study is an in-depth examination of OPCs in the context of both LGG and GBM. Within LGG, our study represents the first examination of OPCs in this disease, and we uncovered compelling evidence that LGGs may arise from OPCs. Within GBM, we identified a novel population of qCSCs with OPC-driven GBM in mouse and human tumors. Additionally, both these efforts establish important preclinical resources for further stratification and study of adult gliomas.