Abstract: The exploration and understanding of myxosporean, one of the crucial stressors causing fish disease, have always been highly regarded. The present study aims to fully understand a novel myxobolid species, Thelohanellus xiushanensis n. sp. infecting the gill filaments of C. auratus from Chongqing, China, as well as the associated pathological impacts. A multifaceted analysis at various levels and perspectives, was carried out by the approach integrating morphology, molecular systematics, histopathology, combined host and habitat, as well as SSU rDNA data. The results indicated that its mature myxospores displayed a tapering anterior and a blunt-rounded posterior, with a drop-shape in front view and melon-seed shape in sutural view in morphology. The outer surface was covered with a transparent membrane sheath in valve view. The dimensions of myxospores were average (19.2 ± 1.1) (17.1 − 21.0) × (10.0 ± 0.7) (8.7 − 12.1) × (9.7 ± 0.5) (9.1 − 10.8) μm. An elliptical polar capsule, containing four to five turns of single polar filament, measures (8.0 ± 0.6) (6.9 − 9.1) × (6.6 ± 0.3) (6.1 − 7.1) μm. Its SSU rDNA sequence demonstrated the closest similarity (99.95%) with an actinosporean Neoactinomyxum sp. NEO-7. Histopathological results indicated that numerous myxoplasmodia of T. xiushanensis n. sp. were located in the tips of the gill filaments, resulting in deformation and rupture of partial gill filaments. Furthermore, severely infected gill lamellae exhibited hyperplasia and fusion, accompanied by infiltration of numorous eosinophils. In addition, regenerated gill filaments were observed at the bases of partially ruptured gill filaments, indicating that the host’s gill tissue has the innate capacity to shed diseased tissues and regenerate new ones. This study has proved the present species and Neoactinomyxum sp. NEO-7 belong to the same myxosporean species but corresponding to different developmental stage, designated as a new species. This novel species is a potential pathogen for the host, which should not be ignored. This study not only enriches myxobolid biodiversity and demonstrates a potentially pathogenic agent, but also provides a valid diagnosis for the gill myxoboliosis caused by the present pathogen in aquaculture.