Adult heart regeneration following infarction is limited by the inability of cardiomyocytes (CMs) to proliferate in response to stress. Therefore, enhancing CM proliferation represents a promising approach for promoting regeneration in the damaged heart. In this context, long noncoding RNAs (lncRNAs) are regulatory molecules controlling cell identity and behavior. We exploited a high throughput-screening assay and neonatal mouse CMs to identify anti-proliferative lncRNAs. Specifically, we used antisense oligonucleotides (GapmeRs) to silence individually 350 novel heart-enriched lncRNAs in CMs and evaluated the impact on proliferation. We identified Clipper, a nuclear enhancer-associated lncRNA located in the Lipin1 locus. GapmeR-mediated Clipper knockdown reduced also Lipin1 expression, indicating that Clipper could work via regulating Lipin1. Interestingly, Lipin1 is a phosphatidic acid phosphatase, controlling a lipid cascade that eventually regulates mitochondrial fission. Two different types of fission events have been previously observed, namely midzone and peripheral fissions, depending on the position of the event along the mitochondrion. Midzone fission is MFF-dependent and associated with proliferation whereas peripheral fission is FIS1-dependent and associated with stress. Upon Clipper knockdown, midzone fissions were increased while peripheral fissions were not affected. Inhibition of midzone fission following Mff knockdown blunted CM proliferation following Clipper silencing, implicating mitochondrial energy metabolism in the process. Clipper knockdown induced a shift from oxidative phosphorylation to glycolysis in proliferating CMs. This was associated with a reduction of ROS production and ROS-induced DNA damage, an important determinant of CM cell cycle arrest. Finally, we evaluated the effects of Clipper knockdown on CM proliferation and heart function in a mouse model of myocardial infraction. CM proliferation, decreased infarct size and improvement of heart function were observed after anti-Clipper GapmeR administration in vivo. Altogether, this study suggests the existence of a coordinated regulation of CM metabolism and proliferation, in part through a Clipper/Lipin1 axis controlling mitochondrial dynamics.