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This study aimed to test the hypothesis of the year-round presence of toxigenic Microcystis and cyanotoxins in the water and ice of the shallow eutrophic Lake Ytyk-Kyuyol located in the continuous permafrost zone. Three independent approaches—mass-spectrometry, molecular methods and light microscopy—were applied in the study. The cyanobacterial biomass ranged from 1.0 × 10−4 to 4.8 mg L−1. Microcystis flos-aquae and M. aeruginosa were the dominant morphospecies in plankton throughout the observation. In environmental DNA, the presence of M. aeruginosa was supported and mcy gene regions responsible for microcystin biosynthesis were detected through a BLAST (Basic Local Alignment Search Tool) search and phylogenetic estimation based on newly obtained 16S rRNA, 16S–23S ITS rRNA, mcyA and mcyE nucleotide sequences. The intracellular microcystin concentration ranged from −1, and the microcystin quota in the Microcystis biomass was extremely low. For the first time, it was shown that Microcystis cells containing mcy genes and microcystins presented permanently in the water column, both during the ice-free period and under ice, as well as inside thick ice covers within 7 months of severe winter. We hypothesized that minor pelagic and ice populations of Microcystis could participate in increasing cell density in the spring. However, further studies are needed to confirm the viability of the overwintering Microcystis colonies in the water and inside the ice of Lake Ytyk-Kyuyol.