Herpesviruses encode conserved protein kinases to optimize virus infection by targeted phosphorylation. How these kinases bind to cellular factors and how this impacts their regulatory functions is poorly understood. Here, we use quantitative proteomics to determine the interactomes of eight herpesvirus kinases. We identify Cyclin A binding as a distinguishing feature of betaherpesvirus kinases that were previously described as viral mimics of cyclin-dependent kinases (v-CDKs), inert to cellular control. RXL motifs within the non-catalytic regions of roseolo- and muromegalovirus v-CDKs serve as Cyclin A docking sites and closely overlap with nuclear localization signals (NLS). By competing with NLS function, Cyclin A binding redirects NLS-RXL containing v-CDKs to cytoplasmic substrates at late times of infection. Concomitantly, Cyclin A is sequestered to the cytoplasm, which is essential for the viral inhibition of cellular DNA replication. Our data highlight a fine-tuned and physiologically important interplay between a cellular cyclin and viral CDK-like kinases.