Cytokinin (CK) is a central regulator of plant development, yet its roles cannot be understood fully without considering how CK signaling was assembled during evolution and redeployed in different physiological contexts. In this review, we examine how prokaryotic two-component modules were elaborated into the land–plant CK system and how this system now integrates biosynthesis, transport, receptor selectivity, and feedback control to shape developmental and symbiotic outcomes. We argue that three recurring interpretive dimensions are especially useful for organizing current evidence: compartmentalized CK pools, context-dependent decoding of local CK availability, and the coupling of local CK responses to whole-plant nutrient status. These dimensions help organize current observations on why CK effects in arbuscular mycorrhiza (AM) are often conditional and readout-dependent, whereas evidence from legume–rhizobium symbiosis supports a more direct role for CK in cortical competence, nodule organogenesis, and autoregulation of nodulation. Rather than treating CK as a generic positive regulator of symbiosis, we propose that it functions as a spatially partitioned and nutritionally gated integrator whose outputs depend on cell type, developmental stage, transport route, and resource context. We conclude by highlighting key mechanistic gaps—particularly in transporter-resolved CK partitioning and systemic integration—and by outlining experimentally testable priorities for translating CK biology into crop improvement.