Clathrin- and actin-mediated endocytosis is a fundamental process in eukaryotic cells. Previously, we discovered Tda2 as a new yeast dynein light chain that works with Aim21 to regulate actin assembly during endocytosis. Here, we show Tda2 functions as a dimerization engine bringing two Aim21 molecules together using a novel binding surface different than the canonical dynein light chain ligand binding groove. Point mutations on either protein that diminish the Tda2-Aim21 interaction in vitro cause the same in vivo phenotype as TDA2 deletion showing reduced actin capping protein recruitment and increased filamentous actin at endocytic sites. Remarkably, chemically induced dimerization of Aim21 rescues the endocytic phenotype of TDA2 deletion. We also uncovered a capping protein interacting motif in Aim21, expanding its function to a fundamental cellular pathway and showing such motif exists outside mammalian cells. Furthermore, specific disruption of this motif causes the same deficit of actin capping protein recruitment and increased filamentous actin at endocytic sites as AIM21 deletion. Thus, the data indicates the Tda2-Aim21 complex functions in actin assembly primarily through capping protein regulation. Collectively, our results provide a mechanistic view of the Tda2-Aim21 complex and its function in actin network regulation at endocytic sites.