Background The importance of the gut microbiota for health and wellbeing is well established for humans and some land animals. The gut microbiota is supposedly as important for fish, but existing knowledge has many gaps, in particular for fish in the Arctic areas. This study addressed the dynamics of Atlantic salmon digesta-associated gut microbiota assemblage and its associations with host responses from freshwater to seawater life stages under large-scale, commercial conditions in the Arctic region of Norway, and explored the effects of functional ingredients. The microbiota was characterized by 16S rRNA gene sequencing in distal intestinal digesta at four time points: 2 weeks before seawater transfer (in May, FW); 4 weeks after seawater transfer (in June, SW1); in November (SW2), and in April (SW3) the following year. Two series of diets were fed, varying throughout the observation time in nutrient composition according to the requirements of fish, one without (Ref diet), and the other with functional ingredients (Test diet). The functional ingredients, i.e. nucleotides, yeast cell walls, one prebiotic and essential fatty acids, were supplemented as single or mixtures based on the strategies from the feed company. Results Overall, the fish showed higher microbial richness and lactic acid bacteria (LAB) abundance after seawater transfer, while Simpson’s diversity decreased throughout the observation period. At SW1, the gut microbiota was slightly different from those at FW, and was dominated by the genera Lactobacillus and Photobacterium. As the fish progressed towards SW2 and SW3, the genera Lactobacillus and Mycoplasma became more prominent, with a corresponding decline in genus Photobacterium. The overall bacterial profiles at these time points showed a clear distinction from those at FW. A significant effect of functional ingredients (a mixture of nucleotides, yeast cell walls and essential fatty acids) was observed at SW2, where Test-fed fish showed lower microbial richness, Shannon’s diversity, and LAB abundance. The multivariate association analysis identified differentially abundant taxa, especially Megasphaera, to be significantly associated with gut immune and barrier gene expressions, and plasma nutrients. Conclusions The gut microbiota profile varied during the observation period, and the Mycoplasma became the dominating bacteria with time. Megasphaera abundance was associated with gut health and plasma nutrient biomarkers. Functional ingredients modulated the gut microbiota profile during an important ongrowing stage.