The F‐actin binding properties of chicken villin, its headpiece and domains 2–3 (V2‐3) have been analysed to identify sites involved in bundle formation. Headpiece and V2‐3 bind actin with K _d values of ~7 μM and ~0.3 μM, respectively, at low ionic strength. V2‐3 binding, like that of villin, is weakened with increasing salt concentration; headpiece binding is not. Competition experiments show that headpiece and V2‐3 bind to different sites on actin, forming the two cross‐linking sites of villin. Headpiece does not compete with the F‐actin binding domains of gelsolin or α‐actinin, but it dissociates actin depolymerizing factor. We suggest that the F‐actin binding domains of actin severing, crosslinking and capping proteins can be organized into two classes.