Global warming is associated with an increase in sea surface temperature and its variability. The consequences of evolving in variable, fluctuating environments are explored by a large body of theory: when populations evolve in fluctuating environments the frequency of fluctuations determines the shapes of tolerance curves (indicative of habitats that organisms can inhabit) and trait reaction norms (the phenotypes that organisms display across these environments). Despite this well-established theoretical backbone, predicting how trait and tolerance curves will evolve in organisms at the foundation of marine ecosystems remains a challenge. Here, we used a globally distributed phytoplankton, Thalassiosira pseudonana, and show that fluctuations in temperature on scales of 3-4 generations rapidly selected for populations with enhanced trait plasticity and elevated thermal tolerance. Fluctuations spanning 30-40 generations selected for the formation of two stable, genetically and physiologically distinct populations, one also evolving high trait plasticity and enhanced thermal tolerance, and the other, akin to samples evolved under constant warming, with lower trait plasticity and a smaller increase in thermal tolerance.