Glioblastoma (GBM) is the most common and lethal form of brain cancer with a one-year survival rate of 12-15 months that is associated with a treatment regimen has not changed in nearly three decades. The development and use of novel immunotherapies such as immune checkpoint inhibitors (ICI) that target and block inhibitory T cell receptors such as Programmed Cell Death Protein 1 (PD-1), was met with initial praise due to its efficacy in a handful of melanoma and lung cancer patients. However, the majority of these patients, including those bearing other solid tumors, such as GBM, fail to respond to ICI. A growing body of literature across different cancer contexts, including GBM, have implicated PI3K signaling with ICI resistance and the formation of an immunosuppressive tumor immune microenvironment (TIME). In GBM, hyperactive PI3K signaling is often a result of amplification or mutations associated with the epidermal growth factor receptor (EGFR) and the deletion or loss of function mutations associated with phosphatase and tensin homologue deleted in chromosome ten (PTEN). Considering that extracellular vesicles (EVs) are able to suppress cytotoxic immune responses and influence the TME, I wondered whether hyperactive PI3K signaling could influence a cancer cell’s ability to upregulate EV biogenesis and/or PD-L1 cargo. Using several isogenic glioma cell lines for EGFRvIII and PTEN expression, I was able to provide convincing evidence that hyperactive PI3K signaling, can lead to both an increase in EV biogenesis and PD-L1 associated cargo. After establishing an in vitro Jurkat reporter system to read out T-cell receptor (TCR) signaling, I then demonstrate that this two-fold change EV associated PD-L1 is functionally superior in reducing TCR signaling in a PD-L1/PD-1 dependent manner. These studies bring new insights into the basic biology and regulation of EVs and also shed new light on how oncogenic PI3K signaling can alter EV function to influence immune evasion and the cultivation of an immunosuppressive TIME.