In mammals, the role played by germ cells in ovarian differentiation and folliculogenesis has been the focus of an increasing number of studies over the last decades. From these studies, it has emerged that bidirectional communication between germ cells and surrounding companion cells is required as soon as the initial assembly of follicles. Models of germ cell depletion that arise from both spontaneous and experimentally induced mutations as well as irradiation or chemical treatments have been helpful in deciphering the role played by germ cells from the onset of ovarian differentiation onward. This review reports current knowledge and proposes novel hypotheses that can be formulated from these models about the contribution of germ cells to ovarian differentiation and folliculogenesis. In particular, it promotes the idea that the influence of germ cells on companion somatic cells varies within both ovarian differentiation and folliculogenesis.