The heart is a highly metabolic organ that uses multiple energy sources to meet its demand for ATP production. Diurnal feeding-fasting cycles result in substrate availability fluctuations which, together with increased energy production during the active period, translate into rhythmic cardiac metabolism. Indeed, pathological cardiovascular events are more common at specific times of the day. The nuclear receptors Rev-erba and -b  are essential components of the molecular circadian clock and major regulators of metabolism. To investigate their role in the heart, we generated mice with cardiomyocyte-specific deletion of both Rev-erbs which, remarkably, died prematurely due to dilated cardiomyopathy. Loss of REV-ERBs markedly dysregulated metabolic genes controlling mitochondrial function in cardiomyocytes prior to overt pathology, which was mediated by induction of the transcriptional repressor E4BP4, a direct target of cardiac REV-ERBs. E4BP4 directly controls circadian expression of Nampt and its biosynthetic product NAD⁺ via distal cis-regulatory elements. Dietary supplementation of CM-RevDKO mice with an NAD⁺ precursor improved cardiac function and extended their lifespan. Thus, REV-ERB-mediated E4BP4 repression is required for Nampt expression and NAD⁺ production by the salvage pathway. Moreover, single nucleus RNA-sequencing revealed transcriptomic remodeling in other cardiac cell types. The cell-specific differentially expressed genes overlapped strikingly with those altered in hearts of patients with dilated cardiomyopathy. These results highlight the indispensable role of circadian REV-ERBs in regulating cardiac energy homeostasis and function, suggest that the gene expression changes due to disruption of the murine molecular clock resemble those of the failing human heart and providing clues as to the cell types from which human disease markers are derived.