Transcription factor fusions are recurrent drivers of sarcomas and other cancers, but their oncogenic reorganization of chromatin is difficult to target. One such fusion, PAX3::FOXO1, drives an aggressive subset of pediatric rhabdomyosarcoma (RMS) through chromatin remodeling, blocking terminal differentiation and sustaining proliferation. We hypothesized that identifying PAX3::FOXO1 genetic dependencies would reveal new facets of transcription factor fusion biology. We report an unexpected role for PAX3::FOXO1 in driving DNA replication fork progression, uncovered by its dependence on the INO80 chromatin remodeling complex (INO80c). Loss of the INO80c member UCHL5 reduces the competitive fitness of fusion positive (FP), but not fusion negative (FN) RMS cell lines, and is accompanied by reduced DNA replication fork speed. UCHL5 is required to maintain the N-terminal subdomain of INO80c, but a catalytically dead UCHL5 is sufficient to rescue complex formation, fork progression, and FP-RMS fitness. Similarly, loss of PAX3::FOXO1 rapidly leads to RPA32 foci and slows DNA fork progression. These findings demonstrate that PAX3::FOXO1 and INO80c are each critical to maintain replication fork progression in FP-RMS, a novel function for this transcription factor fusion. Implications: PAX3::FOXO1 and the N-terminal INO80 complex are both required to drive replication fork progression in FP-RMS, offering a counterpoint to models in which fusion oncogenes drive replication stress, and identifying INO80 complex members as a genetic dependency in FP-RMS cells.