Abnormal sleep and circadian disruption independently alter metabolism and are associated with adverse health risks. Circadian rhythms regulate metabolic and biological processes including sleep-wake cycles. Thus, understanding the metabolic interactions between sleep and circadian processes is of high importance, yet the dynamics of these interactions remain to be discerned. While studies have characterized metabolism in sleep and chronobiology contexts using steady state metabolite measurements, they generally have not been designed to study interactions of circadian and sleep processes. Moreover, steady state measurements provide limited insight into metabolic pathways. Therefore, whether underlying circadian and/or sleep disruption drives the observed metabolic changes remains to be elucidated. To begin addressing this gap, we have harnessed the strengths of Drosophila as a model organism for sleep and circadian processes. Through steady state analyses, we identified altered metabolic pathways during the dark period related to nicotinate and nicotinamide, arginine, and TCA cycle metabolism in short sleep mutants. Following up on the observed steady state changes in energy-related metabolism, we leveraged an in vivo novel metabolic tracing platform to trace glucose carbons into downstream metabolites. Initial work identified differences in glucose processing in wild type and a hyperactive short sleep mutant with phase advanced biosynthesis during the early light period independent of food availability and feeding rhythms. Finally, through optimization of quality control procedures, we were able to more comprehensively profile differences in glucose processing using high time resolution across wild type, clock, and sleep mutants under controlled environmental conditions. These experiments demonstrated conserved increases in downstream glucose biosynthesis (primarily TCA cycle and glycolysis) in short sleep mutants, potentially indicating a conserved metabolic mechanism of sleep loss. Overall, this work begins to detangle the intertwined dynamics of circadian and sleep processes on metabolism and highlights the importance of joint sleep and circadian study designs. The metabolic tracing approach can provide further avenues for exploring time of day differences not only in sleep models but other pathophysiologies with implications on guiding the development of interventions optimized for time of day.