Abstract Glioblastoma (GBM) remains deadly with minimal therapeutic improvement over the past decades. A hallmark of GBM is an immunosuppressive microenvironment, which includes anergic and suppressive T-cells. Antigen presentation is a critical component to successful activation of anti-tumor T cell responses and are dysregulated in GBM. To better understand how GBM cells modulate antigen presenting processes, we examined expression of antigen presentation genes in our single cell RNA-sequencing (scRNA-seq) cohort consisting of 18 GBM samples from 12 different human patients. Unexpectedly, we found a rare population of tumor cells with high expression of CD83, a marker of activated antigen presenting cells (APCs) that stabilizes MHC-II and CD86 expression. In an immunocompetent GFP-labeled piggyBac in utero electroporation (pB-IUE) model of GBM, we validated the existence of dually labeled CD83+GFP+ tumor cells using FACS image streaming. In vivo overexpression of CD83 (CD83OE) in tumor cells prolonged survival compared to control and CD83 knockout (CD83KO) tumors. In vitro, tumor cell lines derived from CD83OE tumors increased expansion and activation of co-cultured CD8+ T-cells whereas CD83KO tumors had a large population of immunosuppressive CD8+ T-cells. ELISAs of media from tumor cell lines revealed that CD83OE tumor cells secrete higher levels of the T cell activating cytokine, IL-2 than controls and CD83KO. scRNA-seq of pB-IUE tumors confirmed that CD83OE have increased activating cytokines compared to CD83KO and control tumors, and that CD83KO tumors had greater expression of immunosuppressive T-regulatory profiles. Intriguingly, we found that despite equal proliferative capacity of tumor cells both in vitro and in vivo conditions, CD83OE tumors were smaller, suggesting that CD83 expression by tumor cells stabilizes CD8+ T-cells to promote immune clearance of tumors. Collectively, our data suggests that enhancing tumor cell expression of antigen presenting markers such as CD83 may encourage immune-mediated clearance of GBM.