Metabolism fuels fundamental biological processes and commonly scales with body mass with an exponent, b, between 2/3 and 1. The Metabolic-level Boundaries Hypothesis (MLBH) predicts that increased activity steepens b. We test this hypothesis by comparing metabolic rates during flight, non-flight locomotion, and rest in winged insects (n = 344), wingless insects (n = 354), and spiders (n = 131). After accounting for phylogenetic relatedness and wing presence, we find interspecific b values vary with activity only in winged insects (resting: 0.78; non-flight: 1.03; flight: 1.06), but not in wingless insects or spiders. Although all arthropods are expected to increase b during activity, this increase occurs only in winged insects, likely due to increased body temperature from muscle energy expenditure. Spiders show a shallower metabolic scaling exponent, potentially due to slowed life history with increasing size. These differences offer new insights into the evolutionary dynamics of arthropod energetics.