Abstract Body: Congenital heart disease (CHD) is a leading cause of birth defects and of all infant deaths. While de novo genetic mutations account for ~10% of CHD, extragenomic factors have a major role. Recent studies showed activated mRNA processing through chemical modification of RNA, termed epitranscriptomics, accounts for a significant proportion of the variance in cellular protein abundance. The most common and conserved epitranscriptomic modification is m6A mRNA methylation. m6A methylation is context dependent, dynamic, and reversible and regulates RNA transport, decay, and translation. However, whether epitranscriptomics play a role in embryonic heart development remains poorly understood. Bioenergetics during cardiogenesis have direct effects on cardiac function and morphogenesis, and disruption of oxidative metabolism results in CHD and lethality. However, the regulatory mechanisms of metabolic adaptations during cardiogenesis remain understudied. To investigate m6A epitranscriptomics during cardiogenesis, we found that both epitranscriptomic writers and m6A mRNA levels peak around mid-gestation. Notably, deletion of the key m6A writer, Methyltransferase 14 (M14-KO), in cardiac progenitor cells resulted in myocardial dysfunction and embryonic lethality. Reduced m6A in cardiac progenitors carries many pathological hallmarks of human CHD, including ventricular non-compaction, reduced cardiomyocyte (CM) proliferation and increased apoptosis. Leveraging single cell RNA-Seq, proteomics and RNA immunoprecipitation-Seq (RIP-Seq), we identified critical m6A modifications in differentially expressed components of the mitochondria electron transport chain (ETC). Importantly, suppression of m6A in a human induced pluripotent stem cell (hiPSC)-based model of cardiac development decreased ETC genes and mitochondria respiration. Moreover, we found that the transcription factor Yin Yang 1 (YY1), has a high stoichiometry of m6A mRNA sites, was a top-upregulated protein in M14-KO hearts and suppressed several metabolic genes in vitro likely acting as an intermediate regulator of oxidative metabolism. Collectively, our findings support that a hallmark metabolic transition during cardiogenesis is controlled by m6A modification of YY1 and key ETC genes.