Abstract Glioblastoma (GBM) is the most common and aggressive primary brain tumor in adults, and causes profound immune suppression both locally and systemically, hindering immunotherapy efficacy. Myeloid-derived suppressor cells (MDSCs) are among the most abundant immune cells in the GBM tumor microenvironment (TME), which exert immune suppression primarily by dampening functional cytotoxic T cells. Extracellular vesicles (EVs) are key mediators of GBM immunosuppression and have been shown to polarize myeloid cells toward immunosuppressive phenotypes, including MDSCs. Inhibition of EV-myeloid cell interactions thus represents a novel strategy to mitigate GBM-mediated immunosuppression. However, the mechanisms of GBM-EVs uptake by myeloid cells are poorly understood. Here, we explored two pharmacological EV uptake inhibitors: Methyl-β-cyclodextrin (MβCD), which disrupts caveolin-mediated endocytosis by depleting membrane cholesterol, and cytochalasin D (CytoD), which impedes phagocytosis via actin depolymerization. Our results showed immunosuppressive myeloid cells (CD11b+/HLA-DRlow/-) and their subset, monocytic MDSCs (mMDSCs) (CD11b+/HLA-DRlow/-/CD14high/CD15-), were induced upon GBM-EV treatment of healthy donor CD11b+ cells. Both inhibitors reduced these populations, with CytoD showing a more pronounced effect (CytoD: 15.01%, MBCD: 16.24% vs. untreated 23.77%) along with partial restoration of T cell proliferation. To validate these findings in vivo, we retro-orbitally injected EVs isolated from the syngeneic murine glioma cell lines GL261 and CT2A into immunocompetent C57BL/6 mice, followed by treatment with either CytoD, MBCD, or vehicle. We observed thymic involution following EV treatment, accompanied by an increase in systemic immunosuppressive myeloid cells in PBMCs and spleen. Both pharmacological inhibitors attenuated these effects, reducing systemic MDSC populations and their suppressive profiles. Our findings highlight that GBM-EVs as key drivers of tumor-mediated immune suppression and demonstrate that targeting EV uptake in myeloid cells is a viable strategy to counteract GBM-mediated immunosuppression.