The shape of many eukaryotic cells depends on the actin cytoskeleton; and localized changes in actin assembly dynamics underlie many changes in cell shape. Polymerases of the Ena/VASP family modulate cell shape by locally accelerating actin filament assembly and slowing filament capping. When concentrated into discrete foci at the leading edge, VASP promotes formation of filopodia, but the mechanisms that drive VASP clustering are poorly understood. Here we show that, in migrating B16F1 cells, VASP molecules assemble on pre-existing foci of the adaptor protein, lamellipodin, and that dimerization of lamellipodin is essential for cluster formation.VASP/lamellipodin clusters grow by accumulating monomers and by fusing, but their growth is limited by a previously undescribed, size-dependent instability. Our results demonstrate that assembly and disassembly dynamics of filopodia tip complexes are determined, in part, by a network of multivalent interactions between VASP, lamellipodin, and actin.