Toxic cyanobacteria, such as Planktothrix rubescens, came to dominate temperate lakes in the mid‐to‐late 20th century, as a result of eutrophication. Even after decades of re‐oligotrophication, where phosphorus levels were reduced by 1–2 orders of magnitude, P. rubescens remains present in various lakes. In this study, we examine the persistence and changes of P. rubescens deep chlorophyll maximum (DCM) in Lake Hallwil (Switzerland) over 35 yr of steadily decreasing phosphorous concentrations. Although lake transparency increased and the euphotic layer deepened during this period, the P. rubescens population maximum moved even deeper. It is now found ca. 7.7 m deeper than its shallowest position in the 2000s, and this depth no longer coincides with the depth of maximal water column stability. P. rubescens neutral buoyancy has now driven it beneath the stable metalimnion into the hypolimnion, where buoyancy regulation is restricted due to reduced metabolic activity at low light and low temperature. If P. rubescens DCM continues to deepen each year, it will eventually reach a region of lower stability in the hypolimnion where turbulent conditions are strong enough to disperse the DCM. We also explore the mechanisms that ensure P. rubescens ongoing presence in peri‐alpine lakes despite strong re‐oligotrophication and ongoing climate change. We find that P. rubescens in the lake is mainly sustained by growth during fully mixed conditions in winter, not during stratification in summer. This may contradict another commonly made prediction that periods of longer stratification will promote future blooms of this cyanobacterium.