Dynactin and NudE/Nudel are prominent regulators of cytoplasmic dynein motility and cargo-binding activities. Both interact with the intrinsically disordered N-terminal domain of dynein intermediate chain (IC)， which also contains phosphorylation sites that apparently regulate these interactions. Nuclear magnetic resonance and isothermal calorimetry studies demonstrate that the Ser84 phosphorylation site identified in cells is in a disordered linker distant from the N-terminal helix that contains both the dynactin- and the Nudel-binding interfaces. Structural studies of a phosphomimetic Ser84Asp imply that phosphorylation stabilizes an electrostatic cluster that docks the disordered linker containing Ser84 against the N-terminal helix， resulting in a conformation that blocks access of IC to dynactin， but not to NudE/Nudel. Formation of this cluster is dependent on the length and sequence of the disordered linkers. This model explains the selective binding of mammalian IC to dynactin versus NudE/Nudel and why this selection is specific for IC-2C and not the IC-1A isoform.