Sliding clamps encircle DNA and tether polymerases and other factors to the genomic template. However, the molecular mechanism of clamp sliding on DNA is unknown. Using crystallography, NMR and molecular dynamics simulations, here we show that the human clamp PCNA recognizes DNA through a double patch of basic residues within the ring channel, arranged in a right-hand spiral that matches the pitch of B-DNA. We propose that PCNA slides by tracking the DNA backbone via a ‘cogwheel’ mechanism based on short-lived polar interactions, which keep the orientation of the clamp invariant relative to DNA. Mutation of residues at the PCNA–DNA interface has been shown to impair the initiation of DNA synthesis by polymerase δ (pol δ). Therefore, our findings suggest that a clamp correctly oriented on DNA is necessary for the assembly of a replication-competent PCNA-pol δ holoenzyme. ; We thank M. Polentarutti and N. Demitri (Elettra Sincrotrone Trieste) for their assistance at the XRD1 beamline, N.G. Abrescia (CIC bioGUNE) and R. Steiner (King’s College, London) for their advice in the crystallographic analysis, and A. Costa (Francis Crick Institute) for his useful comments. This work was supported by the Italian Association for Cancer Research (AIRC iCARE Fellowship to A.De.B. and AIRC Grant IG14718 to S.O.), and the Spanish Ministry of Economy and Competitiveness (CTQ2014-56966-R grant to F.J.B.). S.B.-V. acknowledges a fellowship from the Spanish Ministry of Economy and Competitiveness (Ref. BES-2013-063991). We acknowledge CERIC-ERIC for the use of the XRD1 beamline at Elettra Sincrotrone Trieste. The authors thankfully acknowledge the computer resources, technical expertise and assistance provided by the Red Española de Supercomputación, the Barcelona Supercomputing Center and the Catalan CSUC. ; Peer reviewed