Temperature drives performance and therefore adaptation; to interpret and understand these, thermal performance curves (TPC) are used, often through meta‐analyses, revealing trends across divergent taxa. Four discrete hypotheses—thermodynamic‐constraint; biochemical‐adaptation (hotter is not better); specialist‐generalist; thermal‐trade‐off—have arisen to explain cross‐phyletic trends. In contrast, detailed comparisons of closely related taxa are rare, yet trends arising from these should reveal mechanisms of adaptation, as taxa diverge. Here, we combine experimental work with TPC theory to assess if the current hypotheses apply equally to closely related taxa. We established TPC for six species (and two strains of one species) of the animal model Tetrahymena (Ciliophora)—characterized by SSU rDNA/COX1 sequences—by examining specific growth rate (r), size (V), production (P = rV), and metabolic rate (rV^−0.25) across 15–20 temperatures. Using parameters derived from the mechanistic “Sharpe and DeMichele” function, we established a framework to test which hypothesis best represented the data. We conclude that superficially the “hotter is not better” hypothesis is best but argue that the mechanistic theory underlying it cannot apply at the genus level: trends are likely to arise from little rather than substantial adaptation. Our further analysis suggests: (1) upward shift in the maximum‐functioning temperature (T_max) is more constrained than the optimal temperature (T_opt), leading to a decreased safety margin (T_opt−T_max) and suggesting that species initially succeed in warmer environments through an increase in T_opt, followed by increasing T_max; and (2) thermal performance traits are correlated with phylogeny for closely related species, suggesting that species gradually adapt to new thermal environments.

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