Ciliogenesis requires an orchestrated interaction between the Golgi apparatus and centrioles via vesicle trafficking, yet this process is still poorly understood. Phosphatidylinositol 4-kinase β (PI4KB) is a conserved kinase that localizes to the Golgi for generating phosphatidylinositol 4-phosphate, an important lipid component related to cilium formation. Here, we demonstrate a previously uncharacterized mechanism of PI4KB in regulating Rab11a to enable proper ciliogenesis. PI4KB kinase activity maintains the normal vesicle density around the Golgi and Rab11a localization to centrioles in ciliogenesis. Inhibition of PI4KB activity leads to the reduced centriole localization but accumulation of Rab11a on the Golgi. We identified that the activation of Rab11a relies on PI4KB activity, while inactive Rab11a-guanosine diphosphate stably associates with Golgi and fails to undergo outward delivery. Autosomal-dominant nonsyndromic sensorineural hearing loss mutations in PI4KB abnormally intensify PI4KB interaction with Rab11a, leading to the aberrant subcellular Rab11a localization and defective ciliogenesis. Collectively, our study delineates a critical role for PI4KB in post-Golgi vesicle formation and ciliogenesis.