Water temperature is a key factor in aquaculture production of the commercially valuable sea cucumber Holothuria scabra. Knowledge is scarce about actual energetic costs that can be associated with internal acclimatization processes as a response to thermal extremes. In the present study changes in cellular energy allocation, oxygen consumption rate and energy related enzymes' activity (IDH and LDH) were measured in juvenile H. scabra, held at different temperatures: 21, 27 and 33 °C. The results showed that the steady temperature change (1 °C/day) to both temperature treatments, until reaching the testing temperatures (day 0), clearly affected cellular energy consumption and available energy reserves, measured in the respiratory tree and muscle tissue, respectively. However, 15 and 30 days after acclimation, the initial differences in cellular energy allocation between treatments decreased. In contrast to the variations measured in cellular energy allocation, oxygen consumption was highest at 33 °C and lowest at 21 °C at all three measurement times. Moreover, a significant positive correlation between oxygen consumption rate and temperature was detected at day 15 and day 30. Likewise, a shift from anaerobic to aerobic energy metabolism, indicated by changes in LDH and IDH activities, was observed in the animals from the warm temperature treatment. Results imply that juvenile H. scabra were able to recover from initial disturbances in energy balance, caused by the incremental temperature change of ± 6 °C. Over the experimental period of 30 days, elevated temperature did however, lead to a metabolic shift and more efficient energy turnover, indicated by changes in oxygen consumption rate, LDH and IDH. The synergy of cellular energy allocation and oxygen consumption proved to be a viable indicator to assess the capability of sea cucumbers like H. scabra to cope with extreme temperature conditions. Surprisingly, juvenile H. scabra were able to sustain their energy balance and oxygen consumption rate within the homeostatic range, even at 33 °C. Thus, we assume that rearing temperatures of 33 °C might be possible, which could improve aquaculture production of H. scabra. However, further research is required to understand the mechanisms and effects of acclimation under aquaculture conditions.