Abstract While temperature is well known to affect many life history traits of ectothermic organisms, any attempt to scale up these individual‐level processes to population‐level consequences must assume a relationship between temperature and the strength of per capita density dependence. Yet, theory has made contrasting predictions about this relationship, and we still need clear experimental tests to determine which relationship is realized in natural systems, especially in heterotrophs. Here, we experimentally isolated and quantified the thermal response of density dependence from the population dynamics of the herbivore Daphnia pulex . We show that the strength of negative density dependence increased linearly with temperature, doubling every 7°C, while the intrinsic growth rate of increase showed a humped shape relationship. This difference caused a humped‐shaped relationship of carrying capacity with temperature, with a dramatic 50% decline at the highest temperature. The results provide a sorely needed test of theory and highlight the importance of accounting for thermal responses of indirect effects that only emerge at the population level when forecasting the effects of global warming. While warming temperatures may benefit the individual (via increased growth and reproduction), our results reveal that warming still can be a detriment to the population by strengthening density‐dependent processes.