The fish gill is a vital organ for fish health involved with gas exchange, nitrogen excretion and salt balance. The fish gill is also a chemically diverse environment which hosts a distinct microbiome, yet little is known about its constituents. Here, we describe the nature of the symbiosis between Pacific chub mackerel Scomber japonicus gills and a putative novel species, Shewanella sp., using a combination of whole genome sequencing (WGS) of isolated strains and a broad meta-analysis of 16S rRNA gene amplicon data derived from other marine fish species. It was found that three closely related amplicon sequence variants (ASVs) constituted a median of 30% of the gill microbiome. The successful cultivation of representative isolates matching these environmental ASVs were recovered from mackerel gill samples and whole genomes for these strains were assembled and analyzed. The taxonomy of isolated Shewanella spp. strains was established using a phylogenomic approach. Comparative genomics of diverse Shewanella species highlighted an enrichment of virulence factors in the gill associated Shewanella strains as well as notable loss of function in polyunsaturated fatty acid production, a hallmark characteristic conserved in most members of the genus Shewanella. Finally, meta-analysis of fish gill amplicon data suggests that Shewanella spp. may associate with the gills of forage fishes and provides evidence of trophic transmission to predators of forage fishes.