Dolichospermum is a cyanobacterial genus commonly associated with toxic blooms in lakes and brackish water bodies worldwide, and is a long-term resident of Lake Stechlin, northeastern Germany. In recent decades, shifts in the phosphorus loading and phytoplankton species composition have seen increased biomass of Dolichospermum during summer blooms from 1998, peaking around 2005, and declining after 2020. Cyanobacteria are known to rapidly adapt to new environments, facilitated by genome adaptation. To investigate the changes in genomic features that may have occurred in Lake Stechlin Dolichospermum during this time of increased phosphorus loading and higher biomass, whole genome sequence analysis was performed on samples of ten akinetes isolated from ten, 1 cm segments of a sediment core, representing a ∼45-year period from 1970 to 2017. Comparison of these genomes with genomes of extant isolates revealed a clade of Dolichospermum that clustered with the ADA-6 genus complex, with remarkable genome stability, without gene gain or loss events in response to recent environmental changes. The genome characteristics indicate that this species is suited to a deep-chlorophyll maximum, including additional light-harvesting and phosphorus scavenging genes. Population SNP analysis revealed two sub-populations that shifted in dominance as the lake transitioned between oligotrophic and eutrophic conditions. Overall, the results show little change within the population, despite diversity between extant populations from different geographic locations and the in-lake changes in phosphorus concentrations.