The exact protonation state of cholinesterase active sites remained a puzzle hampering further progress in understanding their structure-function relationships and applied enzyme design studies. In this paper, we systematically explored all possibilities for the number and location of protons within the active site of covalently inhibited hBChE. We established that the balance of two states is typical for this state. A proton may be either on the internal (441) or external (197) Glu residue, and the interconversion is mediated by the water molecule by the Grotthuss mechanism. The same was found true for most of the stages hBChE passes along the native reaction process. In contrast, collapse to mostly one state is a more typical, albeit not only, scenario for hAChE. We compared proton transfer dynamics in hAChE, tcAChE and hBChE, and highlighted the crucial role of the residue Val331 (Asn324, Asn322) in the observed differences. The free energy profile calculated for the inhibited hBChE form on the PBE level suggests a constant dynamical rearrangement of protons or even a system of two conjugated LBHBs. This fine structure of cholinesterase active sites is hard to model correctly with classical MD, therefore we suggest the need of developing ad hoc force field corrections. Our findings generally advance cholinesterase studies and delineate a particularly complex case relevant for the broader field of fundamental enzymology.