Centromeres are essential for genome inheritance, serving as sites for kinetochore assembly and for final sister chromatid cohesion to ensure accurate chromosome segregation during cell division. These roles must persist through radical physical changes to chromosomes and other biological challenges presented by specialized processes in the germlines of both sexes and during early embryonic development. Centromeres in most organisms are epigenetically defined by the presence of a histone H3 variant, CENP-A. Therefore, to maintain centromeres, CENP-A nucleosomes must be inherited across generations through the germline. However, unique aspects of gametogenesis, including asymmetric meiosis and prolonged cell cycle arrest in the female germline and extensive chromatin reorganization in the male germline, introduce additional layers of complexity to the process of centromere inheritance. Here, we review the implications of these processes for centromere regulation during gametogenesis and early embryonic development, drawing on findings from mouse and fruit fly models.