The gill, as vital respiratory organs in fish, maintain direct mucosal contact with aquatic pathogens, wherein their immune system and surface microbiota collectively form a critical defensive barrier.This study established a localized Spring Viremia of Carp Virus (SVCV) infection model in zebrafish to investigate the dynamic responses of gill mucosal immunity and symbiotic microbiota during viral invasion. Viral load, histopathological alterations, and immune-related gene expression profiles were analyzed at multiple post-infection timepoints (1, 4, 7, and 14 days). Results revealed structural disintegration of gill lamellae, respiratory epithelial shedding, and inflammatory cell infiltration following SVCV infection. Concurrently, antiviral genes (ifn-γ,mxc) and pro-inflammatory cytokines (tnfα,il1β) exhibited significant upregulation, particularly during the acute infection phase (4 days post-infection).Integrated transcriptomic and 16S rRNA sequencing further elucidated temporal shifts in mucosal immune pathways and surface microbiota during acute (4 days) and recovery (14 days) phases. Acute infection triggered pronounced inflammatory responses and dysbiosis of the gill microbiota, characterized by proliferation of opportunistic pathogens (e.g.,Pseudomonas) and their translocation into host tissues. This prompted simultaneous activation of systemic and mucosal immune defenses against viral and bacterial co-infections. Notably, both inflammatory signatures and microbiota composition showed partial restoration by the recovery phase.This study demonstrates that SVCV induced gill barrier disruption facilitates microbial dysbiosis and secondary bacterial infections.These findings underscore the necessity for prophylactic measures against bacterial outbreaks during viral epidemics, providing critical insights for the management of Spring Viremia of Carp.