The bacterial adhesin FimH is a model for the study of protein allostery because its structure has been resolved in multiple configurations, including the active and the inactive state. FimH consists of a pilin domain (PD) that anchors it to the rest of the fimbria and an allosterically regulated lectin domain (LD) that binds mannose on the surface of infected cells. Under normal conditions, the two domains are docked to each other and LD binds mannose weakly. However, in the presence of tensile force generated by shear the domains separate and conformational changes propagate across LD resulting in a stronger bond to mannose. Recently, the crystallographic structure of a variant of FimH has been resolved, called FimH ^FocH, where PD contains 10 mutations near the inter-domain interface. Although the X-ray structures of FimH and FimH ^FocH are almost identical, experimental evidence shows that FimH ^FocH is activated even in the absence of shear. Here, molecular dynamics simulations combined with the Jarzinski equality were used to investigate the discrepancy between the crystallographic structures and the functional assays. The results indicate that the free energy barrier of the unbinding process between LD and PD is drastically reduced in FimH ^FocH. Rupture of an inter-domain hydrogen bond involving R166 constitutes a rate limiting step of the domains separation process and occurs more readily in FimH ^FocH than FimH. In conclusion, the mutations in FimH ^FocH shift the equilibrium towards an equal occupancy of bound and unbound states for LD and PD by reducing a rate limiting step.