Microbial diversity and ecology along the marked seasonal contrasts in Arctic waters remain poorly understood. Here, using autonomous sampling, we evaluate community dynamics of bacteria, archaea and microbial eukaryotes over three annual cycles in Fram Strait (Arctic Ocean). We observed marked recurrent seasonality in the ice-free West Spitsbergen Current, with consistent shifts between photoautotrophic and heterotrophic microbes driven by temperature and daylight. However, the major phytoplankton bloomer differed by year, featuring Grammonema (2017), Chaetoceros (2018) and Thalassiosira (2019). Different microbiome patterns in the following winters indicate that the quality and quantity of organic matter depends on phytoplankton bloom dynamics, with cascading effects on heterotrophic nutrient recycling during polar night. The East Greenland Current displayed season-independent community turnover, shaped by variable ice cover and the proportions of Polar water. Our evidence of microbial seasonality in Arctic waters provides an essential baseline of ecosystem dynamics in a region severely affected by climate change, with implications for the present and future Arctic Ocean.