Cells sense external mechanical forces through cadherins (which form cell–cell adhesions) and integrins (which form cell–matrix adhesions). Vinculin (VCL) accumulates at both types of adhesions, where it may exert distinct functions. Bays et al. show that VCL is phosphorylated at Tyr822 in cell–cell adhesions but not in cell–matrix adhesions; applying force to cadherins (but not integrins) increased Tyr822 phosphorylation. Tyr822 phosphorylation has a physiological role, as applying force to cadherins in VCL-knockout cells rescued with wild-type VCL, but not with VCL in which Tyr822 was substituted, enabled cells to stiffen. By contrast, both cell types underwent stiffening when force was applied to integrins. Finally, VCL was phosphorylated at Tyr822 by the Tyr kinase ABL, the activity of which was increased when force was applied to cadherins. Thus, ABL-mediated phosphorylation of VCL at Tyr822 is necessary for cadherins, but not integrins, to transmit force.