Clear cell renal cell carcinoma (ccRCC) is a highly immunogenic tumor and immune dysfunction is associated with ccRCC poor prognosis. The RhoGTPase-activating proteins (RhoGAPs) family was reported to affect ccRCC development, but its role in immunity and prognosis prediction for ccRCC remain unknown. In the current study, we foundARHGAP11Awas the only independent risk factor among 33 RhoGAPs (hazard ratio [HR] 1.949, 95% confidence interval [CI] 1.364–2.785). HighARHGAP11Alevel was associated with shorter overall survival (OS, HR 2.040, 95% CI 1.646–3.417) andARHGAP11Ais a prognostic biomarker for ccRCC.ARHGAP11Aknockdown suppressed renal cell carcinoma (RCC) cell proliferation, colony formation, and migration, suggesting the promoting role ofARHGAP11Aon RCC development. Mechanistically,ARHGAP11Amight contribute to the suppressive tumor immune microenvironment (TIME). HighARHGAP11Alevel was correlated with infiltration of immunosuppressive cells (including T helper 2 (Th2) cells, regulatory T (Treg) cells, myeloid derived suppressor cells (MDSC), and M2 macrophage cells), activation of immunosuppressive pathways (IL6-JAK-STAT3 signaling and IFNγ response), and expression of inhibitory immune checkpoints (ICs).ARHGAP11Acould promote T cell exhaustion and induce immune escape. ccRCC patients with lowARHGAP11Alevel were more suitable for immune checkpoint inhibitors (ICIs) therapy, while those with highARHGAP11Alevel might benefit from a combination ofARHGAP11Ablockade and ICIs. In all,ARHGAP11Amight serve as a novel prognostic marker, therapeutic target, and predictor in the clinical response to ICIs therapy for ccRCC.