A well-orchestrated program of oocyte growth and differentiation results in a developmentally competent oocyte. In late oogenesis, germinal vesicle oocytes (GVOs) undergo chromatin remodeling accompanied by transcriptional silencing from an NSN (non-surrounded nucleolus) to an SN (surrounded nucleolus) chromatin state. By analyzing different cytoplasmic and nuclear characteristics, our results indicate that murine NSN-GVOs transition via an intermediate stage into SN-GVOs in vivo. Interestingly, this transition can also be observed ex vivo, including most characteristics seen in vivo, which allows to analyze this transition process in more detail. The nuclear rearrangements during the transition are accompanied by changes in DNA methylation and Tet enzyme-catalyzed DNA modifications. Early parthenogenetic embryos, derived from NSN-GVOs, show lower DNA methylation levels than SN-derived embryos. Together, our data suggest that a successful NSN-SN transition in oogenesis including proper DNA methylation remodeling is important for the establishment of a developmentally competent oocyte for the beginning of life.