Ectothermic organisms’ respiration rates are affected by environmental temperatures, and sustainable metabolism at high temperatures sometimes limits heat tolerance. Organisms are hypothesized to exhibit acclimatory metabolic compensation effects, decelerating their metabolic processes below Arrhenius expectations based on temperature alone. We tested the hypothesis that either heritable or plastic heat tolerance differences can be explained by metabolic compensation in the eurythermal freshwater zooplankton crustacean Daphnia magna. We measured respiration rates in a ramp-up experiment over a range of assay temperatures (5 °C - 37 °C) in 8 genotypes of Daphnia representing a range of previously reported acute heat tolerances and, in a narrower range of temperatures (10 °C - 35 °C), in Daphnia with different acclimation history (either 10°C or 25°C). We discovered no difference in temperature-specific respiration rates between heat tolerant and heat-sensitive genotypes. In contrast, we observed acclimation-specific compensatory differences in respiration rates at both extremes of the temperature range studied. Notably, there was a deceleration of oxygen consumption at higher temperature in the 25°C-acclimated Daphnia relative to their 10°C-acclimated counterparts, observed in active animals, a pattern corroborated by similar changes in filtering rate and, partly, by changes in mitochondrial membrane potential. A recovery experiment indicated that the reduction of respiration was not caused by irreversible damage during exposure to a sublethal temperature. Response time necessary to acquire the respiratory adjustment to high temperature was lower than to low temperature, indicating that metabolic compensation at the lower temperatures require slower, possibly structural changes.