Actin networks drive cell motility, which is important for essential processes such as embryonic development, wound healing, tissue remodeling, and the immune response. Actin regulatory proteins guide the self-organization of actin into force-generating structures like lamellipodia, filopodia, and ultimately drive cellular motility. Among these regulatory proteins is Capping Protein. Capping protein is a heterodimer that terminates actin filament elongation; it promotes actin network assembly, it competes with Nucleation Promoting Factors (NPF) to bind barbed ends, and is essential for the growth of polarized, force-generating actin networks. How Capping Protein performs these essential functions in the presence of multiple cellular inactivators, V1 and CARMIL, remains a mystery. V1 inactivates Capping Protein, while membrane-bound-CARMIL inhibits Capping Protein. Both the allosteric regulation of Capping Protein by CARMIL and steric inhibition by V1 have been studied from the atomic to the cellular scales. However, the question remains: if CARMIL and V1 inhibit Capping Protein, how does Capping Protein enter the actin network to give rise to cell motility? To answer this question, we used the bead motility assay, which reconstitutes branched actin networks in-vitro with purified components. The assembly of these branched actin networks requires the following key proteins: NPF, the Arp2/3 complex, Profilin, Actin, and Capping Protein. Here, we reconstituted branched actin networks with the addition of the Capping Protein regulators V1 and CARMIL. We immobilized CARMIL on the surface of microbeads to mimic its physiological role, and we used soluble V1 in molar excess with respect to Capping Protein. Our reconstitution assays show that CARMIL, in contradiction to previous work, can activate Capping Protein in the presence of V1 when attached to a surface. In addition, the CARMIL-mediated local activation of Capping Protein also regulates the growth rate and density of branched actin networks. Taken together, our results suggest that CARMIL acts at the cell membrane to activate and deliver Capping Protein to nearby actin filaments, thereby promoting the assembly of force-generating branched actin networks. We further explored the biochemical and biophysical properties of CARMIL, demonstrating its dimeric nature and high-affinity binding to Capping Protein. Using immunofluorescence and scanning electron microscopy, we examined the localization of CARMIL in mammalian cells and its association with purified endosomes. Additionally, we developed CRISPR knock-in strategies to visualize CARMIL endogenously. To complement our experimental findings, we sought agent-based and stochastic models to simulate the dynamic interactions between CARMIL, Capping Protein, and V1, revealing emergent properties in actin network regulation. These experimental and computational approaches offer insights into the self-organization of CARMIL and actin structures while also providing a framework for future investigations of molecular function to explain the emergence of cell motility.