ARID1A, encoding a subunit of the SWI/SNF complex, is the most frequently mutated epigenetic regulator in human cancers and is mutated in over 50% of ovarian clear cell carcinoma (OCCC), a disease that currently has no effective therapy. Inhibition of histone deacetylase 6 (HDAC6) suppresses the growth of ARID1A-mutated tumors and modulates the tumor immune microenvironment. Here we show that inhibition of HDAC6 synergizes with anti-PD-L1 immune-checkpoint blockade in ARID1A-inactivated ovarian cancer. ARID1A directly repressed transcription of CD274, the gene encoding PD-L1. Reduced tumor burden and improved survival was observed in ARID1Aflox/flox/PIK3CAH1047R OCCC mouse treated with the HDAC6 inhibitor ACY1215 and anti-PD-L1 immune-checkpoint blockade as a result of activation and increased presence of interferon-gamma positive CD8 T cells. We confirmed that the combined treatment limited tumor progression in a cytotoxic T-cell-dependent manner as depletion of CD8+ T cells abrogated these antitumor effects. Together, these findings indicate that combined HDAC6 inhibition and immune-checkpoint blockade represents a potential treatment strategy for ARID1A-mutated cancers.