The capacity to compensate for environmental change determines population persistence and biogeography. In ectothermic organisms, performance at different temperatures can be strongly affected by temperatures experienced during early development. Such developmental plasticity is mediated through epigenetic mechanisms that induce phenotypic changes within the animal's lifetime. However, epigenetic modifiers themselves are encoded by DNA so that developmental plasticity could itself be contingent on genetic diversity. In this study, we test the hypothesis that the capacity for developmental plasticity depends on a species' among-individual genetic diversity. To test this, we exploited a unique species complex that contains both the clonal, genetically identical Amazon molly (Poecilia formosa), and the sexual, genetically diverse Atlantic molly (Poecilia mexicana). We predicted that the greater among-individual genetic diversity in the Atlantic molly may increase their capacity for developmental plasticity. We raised both clonal and sexual mollies at either warm (28°C) or cool (22°C) temperatures and then measured locomotor capacity (critical sustained swimming performance) and unforced movement in an open field across a temperature gradient that simulated environmental conditions often experienced by these species in the wild. In the clonal Amazon molly, differences in the developmental environment led to a shift in the thermal performance curve of unforced movement patterns, but much less so in maximal locomotor capacity. In contrast, the sexual Atlantic mollies exhibited the opposite pattern: developmental plasticity was present in maximal locomotor capacity, but not in unforced movement. Thus our data show that developmental plasticity in clones and their sexual, genetically more diverse sister species is trait dependent. This points toward mechanistic differences in how genetic diversity mediates plastic responses exhibited in different traits.