Autotomy, or the voluntary shedding of body parts, is an extreme antipredator behaviour used by species in more than 100 animal families. Despite the long-standing observation that the propensity for autotomy can vary extensively among populations, how ecology might drive such variation is still poorly understood. We tested the hypothesis that the variation in this extreme behaviour reflects the balance between costs and benefits determined by the local ecological environment. We focused on three ecological factors that can influence the cost–benefit dynamics of autotomy: predation, male–male competition, and food abundance. Using tail autotomy in lizards as the study system, we first built an individual-based model to show that environments with high predation, high food abundance, and low male–male competition favoured individuals that autotomized more readily. Moreover, predation likely maintained the ability to autotomize, whereas male–male competition and food abundance fine-tuned the propensity for autotomy. We used field data from five side-blotched lizard populations to verify model results, as well as to test the explanatory power of our model. Field data supported simulation results regarding the roles predation, male–male competition and food abundance. Our model also successfully explained the variation in the propensity for tail autotomy among those five lizard populations. Our approach can be easily extended to examine how ecology might drive adaptive variation in autotomy in other taxa, as well as any traits that share similar cost–benefit dynamics.