Vertebrate oocyte polarity along the animal-vegetal (AV) axis has been observed for two centuries, but how it is generated was unknown. AV oocyte polarity is established by the Balbiani body (Bb), a structure conserved from insects to humans, that contains an aggregate of specific mRNAs, proteins, and organelles. The Bb specifies the oocyte vegetal pole, which is key to forming the embryonic body axes as well as the germ line in most vertebrates. How Bb formation is regulated and how its asymmetric position is established were unknown. Using quantitative image analysis, we traced oocyte symmetry breaking in zebrafish to a nuclear asymmetry at the onset of meiosis called the chromosomal bouquet. The bouquet is a universal feature of meiosis where all telomeres cluster to one pole on the nuclear envelope, facilitating chromosomal pairing and meiotic recombination. We show that Bb precursor components first localize with the centrosome to the cytoplasm adjacent to the telomere cluster of the bouquet. They then aggregate around the centrosome in a specialized nuclear cleft that we identified, assembling the early Bb. We found that the bouquet nuclear events and the cytoplasmic Bb precursor localization are mechanistically coordinated by microtubules. Thus the AV axis of the oocyte is aligned to the nuclear axis of the bouquet. We show that the symmetry breaking events lay upstream to the only known regulator of Bb formation, the Bucky ball protein. Our findings link two universal features of oogenesis, the Bb and the chromosomal bouquet, to oocyte polarization. We propose that a cellular organizer that we term the meiotic–vegetal center, couples meiosis and oocyte patterning. Our findings reveal a novel mode of cellular polarization in meiotic cells whereby cellular and nuclear polarity are aligned. We further revealed that oocytes are organized in cysts where meiotic–vegetal center formation and polarization is synchronized as shown by both live time-lapse and fixed sample data. Moreover, intercellular cytoplasmic bridges remain between oocytes in the cyst and coincide with the location of the centrosome meiotic–vegetal center, suggesting that the last mitotic oogonial division plane positions the centrosome and the meiotic–vegetal center. These results provide the first evidence for a link between polarity and cyst organization. As we show here, the zebrafish ovary provides an excellent genetic model for vertebrate germ cell differentiation, ovarian development and female reproduction.