In this study, we show that two fungal proteins, Aip5 (related to vertebrate SH3BGRL) and Bud6, directly interact to form a novel "composite nucleator," in which the pointed end of a nascent actin seed is bound by the thioredoxin-related domain of Aip5. The Aip5-Bud6 complex assembles F-actin seeds with free barbed ends and recruits formins to processively elongate and protect these ends from capping protein. The nucleation activities of Aip5 and Bud6 are critical for maintaining proper thickness of actin cable bundles in vivo, which prevents premature cable detachment from the bud neck and secretory traffic defects, as revealed by live imaging. In vitro single-molecule imaging reveals that after actin nucleation, Aip5 remains associated with a pointed end of the filament, and in vivo Aip5 puncta are observed directionally streaming inward from polarity sites by actin cable retrograde flow. Our findings expand the known diversity of actin nucleation mechanisms and reveal that Aip5 functions as a pointed-end capper in vivo.