The heritability of genome-wide fitness that is expected in finite populations is poorly understood, both theoretically and empirically, despite its relevance to many fundamental concepts in evolutionary biology. In this study, we used two independent methods of estimating the heritability of lifetime female fecundity (the predominant female fitness component in this population) in a large, outbred population of Drosophila melanogaster that had adapted to the laboratory environment for over 400 generations. Despite strong directional selection on adult female fecundity, we uncovered high heritability for this trait that cannot be explained by antagonistic pleiotropy with juvenile fitness. The evolutionary significance of this high heritability of lifetime fecundity is discussed.