WASP‐family proteins are known to promote assembly of branched actin networks by stimulating the filament‐nucleating activity of the Arp2/3 complex. Here, we show that WASP‐family proteins also function as polymerases that accelerate elongation of uncapped actin filaments. When clustered on a surface, WASP‐family proteins can drive branched actin networks to grow much faster than they could by direct incorporation of soluble monomers. This polymerase activity arises from the coordinated action of two regulatory sequences: (i) a WASP homology 2 (WH2) domain that binds actin, and (ii) a proline‐rich sequence that binds profilin–actin complexes. In the absence of profilin, WH2 domains are sufficient to accelerate filament elongation, but in the presence of profilin, proline‐rich sequences are required to support polymerase activity by (i) bringing polymerization‐competent actin monomers in proximity to growing filament ends, and (ii) promoting shuttling of actin monomers from profilin–actin complexes onto nearby WH2 domains. Unoccupied WH2 domains transiently associate with free filament ends, preventing their growth and dynamically tethering the branched actin network to the WASP‐family proteins that create it. Collaboration between WH2 and proline‐rich sequences thus strikes a balance between filament growth and tethering. Our work expands the number of critical roles that WASP‐family proteins play in the assembly of branched actin networks to at least three: (i) promoting dendritic nucleation; (ii) linking actin networks to membranes; and (iii) accelerating filament elongation. Synopsis WASP‐family proteins activate the Arp2/3 complex to create new actin filaments in branched networks. New data show that these proteins also accelerate elongation of nearby filaments by providing a source of polymerization‐competent actin. Polymerase activity of WASP‐family proteins arises from the recruitment of actin monomers and profilin‐actin complexes to surfaces containing a high density of WASP‐family proteins. Most actin subunits enter a branched filament network via the WASP‐family protein‐coated surface and not directly from solution. Profilin controls whether an actin monomer interacts with the WH2 or the proline‐rich domain of WASP family proteins. Coordination between Proline‐rich and WH2 sequences sets the balance between the network polymerase and tethering activity of WASP family proteins. In addition to creating new actin filaments via the Arp2/3 complex, WASP‐family proteins promote actin filament growth by recruiting actin monomers and actin‐profilin complexes to membrane surfaces.