There are many in vitro tools to measure the amount of force developed by engineered cardiac or skeletal muscle tissues or cells. The work required to generate these forces is normally considered to be equal to the work required to deform the substrate on which the muscle is cultured. However, this approach ignores the amount of energy it takes to generate a constant force with no ongoing substrate deformation, and as a result, drastically underestimates the amount of energy, and therefore the amount of ATP, needed for the contraction. The importance of this contribution to the total work can be easily illustrated by holding aloft a heavy book and feeling muscle fatigue relatively quickly. We hypothesize that the ATP usage during constant loads is driven by fluctuations of the actin-myosin motor inside the basic contractile unit of the muscle—the sarcomere. To test and explore this hypothesis, we built a model of the half sarcomere that can track developed external force and ATP consumption as a function of time. To ensure that the results could be analyzed in situations of varying ATP, ADP, Pi availability, the model was formulated with a physiologically relevant distribution of free energy between the various states of the cross-bridge. The results of our model demonstrate the importance of considering fluctuations when calculating work performed by muscle. Further, the model provides a platform, unavailable with previous sarcomere models, to test the consequences of independently changing the amount of available ATP while at the same time manipulating the amount ADP and Pi present. These results will impact further development of techniques to analyze in vitro force generation by striated muscle.