SummaryAllosteric activation and silencing of leukointegrins transpire through highly complex structural changes between and within domains, mediating integrin affinity and bidirectional allostery relay. However, the landscape of these conformational changes, which is essential for elaborating integrin dynamics on cell surfaces and designing leukointegrin specific small molecules, has not yet been mapped. Herein we combine biophysical approaches and cell-based affinity assays to fine-tune the conformational dynamism and adhesiveness of a leukocyte integrin, αXβ2, using its physiological cofactor Mg2+. Stepwise addition of Mg2+ revealed two mutually coupled events for the αXβ2 ligand-binding domain—called the αX I-domain—corresponding to allostery establishment and affinity maturation. Electrostatic alterations in the statistically co-evolved Mg2+-binding site establish long-range couplings, leading to pH and Mg2+-occupancy dependent bimodal stability change in the αX I-domain fold. The ligand-binding sensorgrams revealed composite affinity events for the αX I-domain accounting for the multiplicity of conformational states existing in the solution. This bi-faceted transition appears to progressively amalgamate the adhesiveness and allostery within the structural interconversion zone. This work highlights how the intrinsically flexible architecture endows a dynamic continuum to the αI-domain structure on the intact integrin platform, thereby progressively regulating allostery establishment and affinity maturation. This dynamic characteristic appears as a specialization of the αX I-domain and is consistent with its rapid equilibration between open and closed conformations, facilitating rapid upregulation of leukocyte adhesiveness and activation.