Marine ectotherms have evolved a range of physiological strategies to cope with temperature changes that persist across generations. For example, metabolic rates are expected to increase following an acute exposure to temperature, with potential detrimental impacts for fitness. However, they may be downregulated in the following generation if offspring experience the thermal conditions of their parents, with a resulting decrease in maintenance costs and fitness maximization. Yet, trans-generational studies on metabolic rates are few in marine ectotherms, thus limiting our ability to accurately predict longer-term implications of ocean warming on organisms' performance, metabolic rates being the fundamental pacemaker for all biological processes. This is particularly true for small-size organisms, for which the determination of individual metabolic rates has been historically challenging, and for many groups of marine invertebrates, such as annelids, which are under-represented in physiological investigations. Here, we exposed the subtidal annelid Ophryotrocha labronica (body length: ~4 mm) to a thermal gradient (21, 24, 26, 29°C) and measured, for the first time in this species, the temperature dependence of metabolic rates across two generations. We found that metabolic rates were positively related to temperature, but this relationship did not differ between generations. Our study provides additional evidence for the diversity of temperature-associated physiological responses of marine ectotherms and offers a number of methodological recommendations for unveiling the mechanisms underpinning the observed trans-generational responses of metabolic rates in marine annelid species.