Germline mutation in mice of the retinoic acid receptor gene RXRα results in a proliferative failure of cardiomyocytes, which leads to an underdeveloped ventricular chamber and midgestation lethality. Mutation of the cell cycle regulator N-myc gene also leads to an apparently identical phenotype. In this study, we demonstrate by chimera analysis that the cardiomyocyte phenotype in RXRα^−/−embryos is a non-cell-autonomous phenotype. In chimeric embryos made with embryonic stem cells lacking RXRα, cardiomyocytes deficient in RXRα develop normally and contribute to the ventricular chamber wall in a normal manner. Because the ventricular hypoplastic phenotype reemerges in highly chimeric embryos, we conclude that RXRα functions in a non-myocyte lineage of the heart to induce cardiomyocyte proliferation and accumulation, in a manner that is quantitatively sensitive. We further show that RXRα is not epistatic to N-myc, and that RXRα and N-myc regulate convergent obligate pathways of cardiomyocyte maturation.