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<i>Vibrio anguillarum</i> is a Gram-negative marine pathogen causative agent of vibriosis in a wide range of hosts, including invertebrates and teleosts. Lumpfish (<i>Cyclopterus lumpus</i>), a native fish of the North Atlantic Ocean, is utilized as cleaner fish to control sea lice (<i>Lepeophtheirus salmonis</i>) infestations in the Atlantic salmon (<i>Salmo salar</i>) aquaculture industry. <i>V. anguillarum</i> is one of the most frequent bacterial pathogens affecting lumpfish. Here, we described the phenotype and genomic characteristics of <i>V. anguillarum</i> strain J360 isolated from infected cultured lumpfish in Newfoundland, Canada. Koch’s postulates determined in naïve lumpfish showed lethal acute vibriosis in lumpfish. The <i>V. anguillarum</i> J360 genome was shown to be composed of two chromosomes and two plasmids with a total genome size of 4.56 Mb with 44.85% G + C content. Phylogenetic and comparative analyses showed that <i>V. anguillarum</i> J360 is closely related to <i>V. anguillarum</i> strain VIB43, isolated in Scotland, with a 99.8% genome identity. Differences in the genomic organization were identified and associated with insertion sequence elements (ISs). Additionally, <i>V. anguillarum</i> J360 does not possess a pJM1-like plasmid, typically present in virulent isolates from the Pacific Ocean, suggesting that acquisition of this extrachromosomal element and the virulence of <i>V. anguillarum</i> J360 or other Atlantic isolates could increase.