Pericentrin (Pcnt) is a multifunctional scaffold protein and mutations in the human PCNT gene are associated with diseases including ciliopathies. Pcnt plays a crucial role in ciliary development in olfactory receptor neurons, but its function in the photoreceptor connecting cilium is unknown. We downregulated Pcnt in the retina ex vivo and in vivo via a virus-based RNA interference approach to study Pcnt function in photoreceptors. ShRNA-mediated knockdown of Pcnt impaired the development of the photoreceptor connecting cilium and outer segment and showed a nuclear migration defect. In protein interaction screens, we found Syne-2 as an interaction partner of Pcnt in photoreceptors. Syne-2, an outer nuclear membrane protein, is important for positioning murine photoreceptor cell nuclei and for centrosomal migration during early ciliogenesis. CRISPR/Cas9 mediated knockout of Syne-2 in cell culture led to an overexpression and mislocalization of Pcnt and to ciliogenesis defects. Our findings suggest that the Pcnt/Syne-2 complex is important for ciliogenesis and outer segment formation during retinal development and plays a role in nuclear migration.