Understanding how the metabolic rate of individual ectotherms changes with temperature (the thermal response curve, TRC) is necessary for predicting how climate change will impact biological systems. With regards to the evolution of the TRC, current theories either assume the existence of insurmountable thermodynamic constraints (e.g., the Metabolic Theory of Ecology), or that these constraints can be overcome through adaptation (e.g., the Biochemical Adaptation hypothesis). In the former case, thermodynamic constraints would give rise to strong correlations between TRC parameters (e.g., rate performance would necessarily increase with optimum temperature). To shed light on this debate, we performed a phylogenetically informed meta-analysis of TRCs of phytoplankton growth rates, while controlling for environmental factors. We detect thermodynamic constraints which, however, are much weaker than expected from the Metabolic Theory of Ecology. We also identify phylogenetically-independent environmental associations of thermal parameters (e.g., the thermal optimum decreases with absolute latitude), but these vary across species groups (e.g., all phytoplankton vs. only marine species). Overall, our study suggests that the thermal response curves of phytoplankton evolve largely in the absence of hard constraints, and are seemingly able to adapt to the conditions of the local environment.