Atlantic salmon (Salmo salar) farmed in seawater in Tasmania can experience temperatures close to their thermotolerance limit during summer and bacteria of the family Vibrionaceae are a major component of their gut microbiome. Multiyear survey and co-occurrence network analyses confirmed novel members of genus Aliivibrio reliably colonise the gut microbiome in Atlantic salmon farmed in marine pens in Tasmania when the confounding influences of DNA and bacteria from feed and water was taken into account. Aliivibrio and Mycoplasma were the main taxa found to colonise the hind gut mucosal layer. Warm water temperature(19°C) experiments performed in seawater tanks indicated Aliivibrio and Vibrio rapidly become predominant in the digesta of Atlantic salmon that had reduced feeding and high faecal cast production while Mycoplasma were mostly absent. The main salmon-associated Aliivibrio isolates were found to share many genes required for host colonisation with the faunal mutualist Aliivibrio fischeri. Tasmanian Atlantic salmon strains, however, possess a range of different colonisation-enabling mechanisms and virulence factors, such as cytolethal distending toxin. Interactions between different Vibrionaceae in the gut of Atlantic salmon could be important for overall fish health, especially when they are exposed to stressful conditions, such as elevated sea surface temperatures.