The functional diversity of microbes along the seasonal extremes in the Arctic Ocean including the Polar Night are virtually unknown. Here, using PacBio long-read metagenomes derived from automated samplers over an annual cycle, we elucidate functional microbial seasonality in the Fram Strait in the context of a high-resolution amplicon time-series. In the ice-free West Spitsbergen Current, the transition from the phototrophy-dominated spring and summer ecosystem states to the dark winter was evident in bacterial genomes. Proteorhodopsin- and DMSP-utilizing genes peaked in late summer, marking a transition phase. Winter mixing of the water column covaried with microbial taxa encoding ammonia- and urea-metabolizing genes, with probable implications for nitrogen recycling and the following phytoplankton bloom. In the ice-covered East Greenland Current, functional diversity varied with the extent of ice cover and polar water masses. During intermittent low-ice conditions in winter, the metagenomic repertoire resembled that during summer, indicating rapidly (i.e. within weeks) shifting ecosystem states with ice cover. Overall, we provide a baseline to understand ecological and biogeochemical processes in a region severely affected by climate change, with implications for the present and future Arctic Ocean.