Glioblastomas (GBMs) are lethal primary malignant brain tumors characterized by high treatment resistance, immunosuppression and invasiveness. Fibroblast growth factor-inducible 14 (Fn14) is a cell surface receptor belonging to the TNF receptor superfamily. Fn14 overexpression can drive receptor-autonomous signaling in glioma cells, increase brain invasion and tumor-associated macrophages/microglia (TAMMs) recruitment and correlates with reduced survival in GBM patients and murine glioma models. While prior studies report Fn14 expression in non-tumor cells within the GBM tumor microenvironment (TME), their contributions to glioma pathobiology remain unclear. In this study, we examined the role of Fn14 in glioma biology and survival using tumor-host pairings of Fn14-positive and -knockout (-KO) cells and mice. Cellular and molecular analyses of mouse gliomas and transcriptomic analysis of human GBM datasets was performed to assess Fn14-associated changes in the glioma TME and subject outcomes. Our in vitro studies revealed that Fn14 depletion from glioma cells alters their proliferation and migration and significantly diminishes their self-renewal capacity. Fn14 was found to be highly expressed in tumor cells and TAMMs in human GBM and in the two well-characterized murine glioma models used in this study. We found that Fn14 deletion in both murine tumor and host cells enhanced animal survival. Notably, this survival benefit was stronger in the glioma model with a more immunologically activated TME. Immunophenotyping of mouse gliomas revealed that Fn14 loss reshapes the immune landscape, reducing the infiltration of immunosuppressive macrophages and exhausted T-cells, suggesting that Fn14 modulates both innate and adaptive immune responses. These findings were supported and validated by analyses of human GBM datasets, where high Fn14 expression correlated with immunosuppressive shifts and poor patient responses to immune checkpoint inhibitor therapy. This study is the first to reveal previously unknown contributions of both tumor and host Fn14 expression and removal on survival and identifies Fn14 as a mediator of innate and adaptive immunity in gliomas. The findings presented here indicate that depleting or inhibiting Fn14 in GBM patients with Fn14-high expressing tumors could be a promising approach to reduce immunosuppression and improve responses to immunotherapy.