Abstract Small-bodied ectotherms are acutely vulnerable to temperature changes but diverse thermotactic behaviours have contributed to their ability to inhabit broad climatic niches. Understanding how - and how fast - these behaviours evolve are outstanding biological questions that are also relevant to conservation. Among insects, Drosophila melanogaster is a preeminent ectothermic model for temperate sensing and thermotaxis. However, little is known about how its temperature-related behaviours have evolved in comparison to its closely-related species. We have thermo-profiled over ∼2400 larvae from eight closely related species of Drosophila from different thermal habitats. We found substantial variation in temperature preference and fine-scale navigational behaviours amongst these species, consistent with local adaptation. Agent-based modelling of the larval thermotaxis circuit indicate that it is the balance between cool and warm avoidance circuits, rather than changes in temperature sensitivity, that drive differences in temperature preference. Together, our findings highlight the fast evolution of temperature-related behaviours in an experimentally tractable cross-species system.

Fast and recurrent evolution of temperature preference among drosophilids