Significance The discovery that more than 40% of the eukaryotic proteome is intrinsically disordered, and that these disordered segments are enriched in phosphorylation sites, suggests that conformational heterogeneity may be important to kinase selectivity. Indeed, phosphorylation prediction programs reliant on classic notions of conserved sequence information (i.e., “vertical information”) are only partially effective. We find that the conformational equilibrium of the phosphorylatable site, whose information is embedded in sequence-averaged energetic and structural properties of the protein (i.e., “horizontal information”), plays a major role in distinguishing phosphorylatable versus nonphosphorylatable sites. In fact, employing both horizontal and vertical information produces a state-of-the-art phosphorylation predictor, wherein the conformational equilibrium of the disordered chain is the dominant contributor.