Mitochondria undergo architectural/functional changes in response to metabolic inputs. How this process is regulated in physiological feeding/fasting states remains unclear. Here we show that mitochondrial dynamics (notably fission and mitophagy) and biogenesis are transcriptional targets of the circadian regulator Bmal1 in mouse liver and exhibit a metabolic rhythm in sync with diurnal bioenergetic demands. Bmal1 loss-of-function causes swollen mitochondria incapable of adapting to different nutrient conditions accompanied by diminished respiration and elevated oxidative stress. Consequently, liver-specific Bmal1 knockout (LBmal1KO) mice accumulate oxidative damage and develop hepatic insulin resistance. Restoration of hepatic Bmal1 activities in high-fat-fed mice improves metabolic outcomes, whereas expression of Fis1, a fission protein that promotes quality control, rescues morphological/metabolic defects of LBmal1KO mitochondria. Interestingly, Bmal1 homolog AHA-1 in C. elegans retains the ability to modulate oxidative metabolism and lifespan despite lacking circadian regulation. These results suggest clock genes are evolutionarily conserved energetics regulators. Display omitted •Bmal1 controls rhythmic mitochondrial dynamics gene expression in the liver•The dynamic mitochondrial activity manages metabolic flexibility and oxidative stress•Bmal1 depletion causes enlarged, dysfunctional mitochondria and hepatic pathologies•C. elegans Bmal1 homolog AHA-1 regulates oxidative metabolism and extends lifespan Mitochondrial dynamics plays an important role in metabolic adaptation to nutrient influx. Jacobi et al. reveal that the circadian regulator Bmal1 controls rhythmic mitochondrial dynamics gene expression in the liver. Hepatic Bmal1 gene deletion causes abnormal mitochondrial morphology, elevated oxidative damage, and metabolic inflexibility.