Kaposi’s sarcoma-associated herpesvirus (KSHV) is an oncogenic gammaherpesvirus with a biphasic life cycle. KSHV infection of oral epithelial cells supports lytic replication and transmission into B cells where viral genome heterochromatinization drives KSHV into latency. Epigenetic factors that counteract heterochromatin could thus be targets to block lytic infection. Here, we evaluated the role and regulation of host BRCA1 associated protein (BAP1) in KSHV’s life cycle. BAP1 deubiquitinates H2AK119Ub, a repressive mark abundant on latent KSHV genomes, but its role during infection is unknown. BAP1 can also function as a scaffold to recruit histone methyltransferase MLL3 complexed with histone demethylase UTX and acetyltransferase CBP to support host gene transcription via removal of H3K27me3 and H3K27Ac deposition, respectively. We hypothesized that BAP1 might support KSHV’s lytic cycle as an enzyme or a scaffold leading to KSHV euchromatinization. We found that siRNA-mediated depletion of BAP1 in telomerase-immortalized gingival keratinocytes (TIGKs) reduced viral gene expression and KSHV copy number at 24 hours post-infection (hpi). Inhibiting BAP1 enzymatic activity did not affect H2AK119Ub levels at lytic promoters nor lytic gene expression, while BAP1 depletion resulted in increased H3K27me3 and decreased H3K27Ac marks at lytic promoters. MLL3 depletion in TIGKs inhibited lytic infection, in support of a functional BAP1/MLL3 axis. Strikingly, immunofluorescence revealed that BAP1 highly accumulates during de novo KSHV infection in the nucleus of TIGKs expressing lytic proteins, but not in adjacent infected cells that lack lytic proteins. Conversely, depletion of BAP1 did not impair lytic infection by Herpes simplex virus (HSV-1) in TIGKs, indicating that the requirement for BAP1 is virus-specific. In summary, we propose that BAP1 may be co-opted specifically by KSHV and tethered to the KSHV genome during lytic infection to recruit MLL3 complexes to promote lytic infection.