Significance Assembly of actin filaments near the plasma membrane drives extension of the cell edge as it migrates. Cells recruit a protein machine called the Arp2/3 complex to the leading edge to initiate actin filament branches that grow and push on the membrane. Equally important, capping protein (CP) binds to and terminates polymerization of the fast-growing end of the filament. Like other aspects of actin assembly, CP is subject to regulation. Specifically, the protein V-1/myotrophin inactivates CP, while capping protein Arp2/3 myosin I linker (CARMIL) proteins moderately inhibit CP. We describe how CARMIL and V-1 cooperate in a cycle of reactions to regulate CP and promote assembly of the actin network by the Arp2/3 complex.