During postnatal heart development in mice, the ventricular myocardium undergoes extensive remodeling with increased organization and maturation of cardiomyocytes, fibroblasts and endothelial cells. In addition, the cardiomyocytes transition from hyperplastic to hypertrophic growth, while losing regenerative capacity. Fibroblast diversity and contributions to heart maturation were examined for periostin (Postn) and Tcf21-expressing cell lineages. A subpopulation of highly proliferative Postn+ cardiac fibroblasts is present in the neonatal heart at postnatal day (P)1 to P11 but is not detected at P30. This population is less abundant and transcriptionally different from Tcf21+ resident cardiac fibroblasts, which persist in the mature heart. The Postn+ subpopulation preferentially expresses genes related to cell proliferation and neuronal development, while Tcf21+ cardiac fibroblasts differentially express genes related to ECM maturation at P7 and immune crosstalk at P30. A subpopulation of the Postn+ cells express Schwann cell markers and ablation of the Postn+ cardiac fibroblasts from P0 to P6 leads to reduced fasciculation of cardiac sympathetic nerves. In addition, ablation of Postn+ cardiac fibroblasts leads to a reduction in cardiomyocyte binucleation, cell cycling, and hypertrophic growth, supporting a non-cell autonomous role for fibroblasts in maturation of postnatal cardiomyocytes. Together, postnatal cardiac fibroblasts are heterogeneous and include a transient proliferative Postn+ subpopulation required for cardiac nerve development and cardiomyocyte maturation soon after birth.