Meiosis is a cellular program essential for the production of haploid gametes. A hallmark of meiosis is chromosomal pairing via synaptonemal complexes, and a major focus traditionally has been to understand synaptonemal complex formation. However, chromosomal pairing also depends on cytoplasmic counterparts that tether and rotate telomeres on the nuclear envelope, shuffling chromosomes and mechanically driving their homology searches. Rotating telomeres slide on perinuclear microtubules and are ultimately pulled towards the centrosome, forming a configuration called the zygotene chromosomal bouquet. The bouquet is universally conserved and is essential for pairing and fertility. However, despite its discovery in 1900, how the cytoplasmic counterparts of bouquet formation are mechanically regulated has remained enigmatic. Here, by studying zebrafish oogenesis, we report and comprehensively characterize a previously unrecognized cilium in oocytes, which we term the zygotene cilium. We show that the zygotene cilium specifically connects to the bouquet centrosome and constitutes a cable system of the cytoplasmic bouquet machinery. Farther, zygotene cilia extend throughout the germline cyst, a conserved cellular organization of germ cells. By analyzing multiple ciliary mutants, we demonstrate that the zygotene cilium is essential for chromosomal pairing, germ cell morphogenesis, ovarian development and fertility. We further show that the zygotene cilium is conserved in both male meiosis in zebrafish, as well as in mammalian oogenesis. Our work uncovers the novel concept of a cilium as a critical player in meiosis and sheds new light on reproduction phenotypes in ciliopathies. Furthermore, most cells in metazoans are ciliated and exhibit specific nuclear dynamics. We propose a cellular paradigm that cilia can control chromosomal dynamics.