Abstract The Arctic Ocean is experiencing unprecedented changes because of climate warming, necessitating detailed analyses on the ecology and dynamics of biological communities to understand current and future ecosystem shifts. Here, we generated a four-year, high-resolution amplicon dataset along with one annual cycle of PacBio HiFi read metagenomes from the East Greenland Current (EGC), and combined this with datasets spanning different spatiotemporal scales (Tara Arctic and MOSAiC) to assess the impact of Atlantic water influx and sea-ice cover on bacterial communities in the Arctic Ocean. Densely ice-covered polar waters harboured a temporally stable, resident microbiome. Atlantic water influx and reduced sea-ice cover resulted in the dominance of seasonally fluctuating populations, resembling a process of “replacement” through advection, mixing and environmental sorting. We identified bacterial signature populations of distinct environmental regimes, including polar night and high-ice cover, and assessed their ecological roles. Dynamics of signature populations were consistent across the wider Arctic; e.g. those associated with dense ice cover and winter in the EGC were abundant in the central Arctic Ocean in winter. Population- and community-level analyses revealed metabolic distinctions between bacteria affiliated with Arctic and Atlantic conditions; the former with increased potential to use bacterial- and terrestrial-derived substrates or inorganic compounds. Our evidence on bacterial dynamics over spatiotemporal scales provides novel insights into Arctic ecology and indicates a progressing Biological Atlantification of the warming Arctic Ocean, with consequences for food webs and biogeochemical cycles.