White gill disease (WGD) is one of the major diseases affecting Larimichthys crocea, although its etiology remains unclear. To investigate the causes of WGD, this study selected WGD-affected Larimichthys crocea (WG) and healthy Larimichthys crocea (NH) from multiple aquaculture regions for pathological analysis and analysis of bacterial and viral community characteristics. The results indicated severe tissue damage and significant inflammatory responses, as evidenced by clinical manifestations and electron microscopy. Two bacterial species, Photobacterium damselae and Vibrio campbellii, were isolated from all lesion tissues. Additionally, 16S full-length sequencing results showed that Photobacterium damselae and Vibrio campbellii dominated in the tissues of Larimichthys crocea, with a combined relative abundance of approximately 90%. There were no significant differences in α-diversity and β-diversity between the NH group and WG group from the three aquaculture regions, and no significant biomarkers were identified. The diversity of DNA and RNA viruses did not show significant differences between the NH and WG groups, although both types of viruses exhibited notable synergistic and antagonistic relationships. Analyses from 16S full-length sequencing, metagenomics, and metatranscriptomics revealed that the related functional genes were primarily enriched in various metabolic pathways, including glycine biosynthesis, membrane transport, and energy metabolism. The metatranscriptomic analysis indicated that the expression levels of genes related to antibiotic resistance, biosynthesis, transport, and degradation processes were significantly downregulated in the WG group. Finally, through PCR, qPCR, and metagenomic sequencing, we were unable to detect iridovirus in Larimichthys crocea, further suggesting that the causes of WGD may differ across aquaculture regions compared to previous reports. This study indicates that the etiology of WGD may involve complex ecological and metabolic mechanisms, rather than being merely the result of a single pathogen infection. This research provides a comprehensive analysis of the microbial communities in WGD-affected Larimichthys crocea from multiple aquaculture regions for the first time, providing a theoretical basis for further elucidating the causes of WGD and developing preventive measures.