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Cunner (<i>Tautogolabrus adspersus</i>) is a cleaner fish being considered for utilized in the North Atlantic salmon (<i>Salmo salar</i>) aquaculture industry to biocontrol sea lice infestations. However, bacterial diseases due to natural infections in wild cunners have yet to be described. This study reports the isolation of <i>Pseudomonas</i> sp. J380 from infected wild cunners and its phenotypic, genomic, and transcriptomic characterization. This Gram-negative motile rod-shaped bacterium showed a mesophilic (4–28 °C) and halotolerant growth. Under iron-limited conditions, <i>Pseudomonas</i> sp. J380 produced pyoverdine-type fluorescent siderophore. Koch’s postulates were verified in wild cunners by intraperitoneally (i.p.) injecting <i>Pseudomonas</i> sp. J380 at 4 × 10³, 4 × 10⁵, and 4 × 10⁷ colony forming units (CFU)/dose. Host-range and comparative virulence were also investigated in lumpfish and Atlantic salmon i.p. injected with ~10⁶ CFU/dose. Lumpfish were more susceptible compared to cunners, and Atlantic salmon was resistant to <i>Pseudomonas</i> sp. J380 infection. Cunner tissues were heavily colonized by <i>Pseudomonas</i> sp. J380 compared to lumpfish and Atlantic salmon suggesting that it might be an opportunistic pathogen in cunners. The genome of <i>Pseudomonas</i> sp. J380 was 6.26 megabases (Mb) with a guanine-cytosine (GC) content of 59.7%. Biochemical profiles, as well as comparative and phylogenomic analyses, suggested that <i>Pseudomonas</i> sp. J380 belongs to the <i>P. fluorescens</i> species complex. Transcriptome profiling under iron-limited vs. iron-enriched conditions identified 1159 differentially expressed genes (DEGs). Cellular metabolic processes, such as ribosomal and energy production, and protein synthesis, were impeded by iron limitation. In contrast, genes involved in environmental adaptation mechanisms including two-component systems, histidine catabolism, and redox balance were transcriptionally up-regulated. Furthermore, iron limitation triggered the differential expression of genes encoding proteins associated with iron homeostasis. As the first report on a bacterial infection in cunners, the current study provides an overview of a new marine pathogen, <i>Pseudomonas</i> sp. J380.