Physiology is regulated by interconnected cell and tissue circadian clocks. Disruption of the rhythms generated by the concerted activity of these clocks is associated with metabolic disease. Here we tested the interactions between clocks in two critical components of organismal metabolism, liver and skeletal muscle, by rescuing clock function either in each organ separately or in both organs simultaneously in otherwise clock-less mice. Experiments showed that individual clocks are partially sufficient for tissue glucose metabolism, yet the connections between both tissue clocks coupled to daily feeding rhythms support systemic glucose tolerance. This synergy relies in part on local transcriptional control of the glucose machinery, feeding-responsive signals such as insulin, and metabolic cycles that connect the muscle and liver. We posit that spatiotemporal mechanisms of muscle and liver play an essential role in the maintenance of systemic glucose homeostasis and that disrupting this diurnal coordination can contribute to metabolic disease. Display omitted •Muscle Bmal1 is partially sufficient to drive local glucose metabolism•Diurnal transcriptomes of liver and muscle are largely independent•Even in combination, liver and muscle clocks do not impart systemic glucose tolerance•Synergy between feeding rhythms and liver and muscle clocks enables glucose tolerance Smith et al. rescued circadian clock function in liver and muscle in otherwise clock-less mice, finding that glucose tolerance is achieved only when feeding rhythms and Bmal1 function in liver and muscle are engaged simultaneously. The authors posit that disruption of this spatiotemporal mechanism contributes to circadian-disruption-induced metabolic disease.