Parasitic diseases are considered to be a major problem in olive flounder (Paralichthys olivaceus) farms in South Korea, with scuticociliate infections being especially problematic due to their year-round occurrence and difficulty in control. In this study, we collected scuticociliates from flounder showing typical symptoms of scuticociliasis, such as ulcers, hemorrhages, and necrosis, at farms in Busan and Jeju, South Korea. Four species of scuticociliates were identified: Mesanophrys carcini, Miamiensis avidus, Paralembus digitiformis, and Pseudocohnilembus persalinus, the M. carcini and P. digitiformis being recorded for the first time in this study. Pathogenicity tests on healthy and wounded fish revealed that M. avidus was highly lethal, while the other species had minimal effects on healthy fish. However, P. digitiformis and P. persalinus impeded wound healing and showed high infection rates in wounded fish without causing high mortality. These two species also triggered early up-regulation of stress-related genes, such as complement C3, followed by a decrease in pro-inflammatory cytokine expression in the olive flounder. These findings emphasize the varied pathogenicity depending on scuticociliate species and suggest that, in addition to the known scuticociliates such as M. avidus, other potential parasites may pose significant risks to olive flounder farms in South Korea.