In this work, a comprehensive analysis of the local geometrical and physicochemical properties of a type III allosteric pocket located between the regulatory αC helix and the activation loop of protein kinases was made by comparing available crystal structures in the structural kinome. We first explored the structural kinome to outline the possible conformations of this site. Subsequently we characterized the positions of cocrystallized ligands of the structural kinome with respect to the structural variability of the allosteric site. Then, we searched for kinase structures with similar allosteric site conformation. The search returned 26 kinases with a DFG-in/αC-out conformation potentially prone to bind allosteric inhibitors, as well as different scaffolds that can be useful starting points for the design of new inhibitors. These promising allosteric pockets were probed by performing molecular docking of known active compounds taken from ChEMBL. Interestingly, none of the active compounds reported in ChEMBL had a purely allosteric binding mode, and none of the ATP-competitive ligands had chemical moieties extending into the allosteric pocket in more than two-thirds of the investigated kinases, indicating that the allosteric pocket is accessible but still largely unexplored by available inhibitors. Finally, we compared the physicochemical properties of the allosteric site in the structural kinome and discussed the peculiar and conserved features. These analyses may help the design of allosteric ligands tailored toward the intended kinase(s).