Mathematical models that incorporate the temperature dependence of lab-measured life history traits are increasingly used to predict how climatic warming will affect ectotherms, including disease vectors and other arthropods. These temperature-trait relationships are typically measured under laboratory conditions that ignore how conspecific competition in depleting resource environments—a commonly occurring scenario in nature—regulates natural populations. Here, we used laboratory experiments on the mosquito Aedes aegypti, combined with a stage-structured population model, to show that intensified larval competition in ecologically-realistic depleting resource environments can significantly diminish the vector’s maximal population-level fitness across the entire temperature range, cause a 6°C decrease in the optimal temperature for fitness, and contract its thermal niche width by 10°C. Our results provide evidence for future studies to consider competition dynamics under depleting resources when predicting how eukaryotic ectotherms will respond to climatic warming.