Using spatially explicit, stochastically kinetic, molecular models of muscle force generation, we examined the relationship between mechanical power output and energy utilization under differing patterns of length change and activation. A simulated work loop method was used to understand prior observations of sub-maximal power output in the dominant flight musculature of the hawkmoth Manduca sexta L. Here we show that mechanical work output and energy consumption (via ATP) vary with the phase of activation, although they do so with different phase sensitivities. The phase relationship for contraction efficiency (the ratio of power output to power input) differs from the phase relationships of energy consumption and power output. To our knowledge, this is the first report to suggest that ATP utilization by myosin cross-bridges varies strongly with the phase of activation in muscle undergoing cyclic length changes.