Conformational landscapes of the Hsp90 chaperones have revealed that the intrinsic plasticity and functional adaptability of these molecular chaperones to a large cohort of cochaperones and a vast protein clientele can be regulated by a number of single switch points broadly dispersed in the chaperone structure. A detailed dynamic view of the allosteric changes mediated by conformational switches and the mechanism of their coupling during the ATPase cycle remains poorly understood and presents an important area of investigation. In this work, we employed integrative computational modeling that included evolutionary and coevolutionary analyses, experiment-guided protein docking and structure modeling, molecular simulations, energetic analysis, and network modeling to perform a systematic characterization of molecular and network signatures of conformational switch points and dissect their allosteric cross-talk in the Hsp90 complexes with cochaperones and client proteins. Using a hierarchical modeling of dynamic interaction networks, we show that the allosteric regulation of the Hsp90 interactions with p23 and Aha1 cochaperones and p53 client protein may be determined by the intramolecular communication "spines" of spatially separated and allosterically coupled regulatory switches. Using a battery of computational approaches, we examined how p23, Aha1, and p53 proteins can modulate signal transmission in the Hsp90 by exploiting communication spines of regulatory switches in the global allosteric network. This study proposes a community-chain mechanism of allosteric coupling between conformational switch centers and identifies key regulatory control points that mediate long-range interactions and communications in the Hsp90 chaperone. The results of this investigation provide novel insights into the nature of allosteric regulation mechanisms in the Hsp90 chaperones and offer a simple mechanistic model of the Hsp90 communications and adaptation to binding partners during the functional cycle.