Reflecting its pleiotropic functions, Polo-like kinase 1 (PLK1) localizes to various sub-cellular structures during mitosis. At kinetochores, PLK1 contributes to microtubule attachments and mitotic checkpoint signaling. Previous studies identified a wealth of potential PLK1 receptors at kinetochores, as well as requirements for various mitotic kinases, including BUB1, Aurora B, and PLK1 itself. Here, we combine ectopic localization, in vitro reconstitution, and kinetochore localization studies to demonstrate that most and likely all of the PLK1 is recruited through BUB1 in the outer kinetochore and centromeric protein U (CENP-U) in the inner kinetochore. BUB1 and CENP-U share a constellation of sequence motifs consisting of a putative PP2A-docking motif and two neighboring PLK1-docking sites, which, contingent on priming phosphorylation by cyclin-dependent kinase 1 and PLK1 itself, bind PLK1 and promote its dimerization. Our results rationalize previous observations and describe a unifying mechanism for recruitment of PLK1 to human kinetochores. © 2020 The Author(s) Polo-like kinase 1 (PLK1) targets kinetochores to regulate microtubule attachment and mitotic checkpoint signaling. Singh et al. show how CDK1 and PLK1 promote kinetochore recruitment and dimerization of PLK1 onto BUB1 and CENP-U, probably the only PLK1 receptors in the core kinetochore. A conserved constellation of docking sites in BUB1 and CENP-U, including one for PP2A phosphatase, suggests a common regulatory switch. © 2020 The Author(s)