In prevailing epithelial polarity models, membrane- and junction-based polarity cues such as the partitioning-defective PARs specify the positions of apicobasal membrane domains. Recent findings indicate, however, that intracellular vesicular trafficking can determine the position of the apical domain, upstream of membrane-based polarity cues. These findings raise the question of how vesicular trafficking becomes polarized independent of apicobasal target membrane domains. Here, we show that the apical directionality of vesicle trajectories depends on actin dynamics during de novo polarized membrane biogenesis in theC. elegansintestine. We find that actin, powered by branched-chain actin modulators, determines the polarized distribution of apical membrane components, PARs, and itself. Using photomodulation, we demonstrate that F-actin travels through the cytoplasm and along the cortex toward the future apical domain. Our findings support an alternative polarity model where actin-directed trafficking asymmetrically inserts the nascent apical domain into the growing epithelial membrane to partition apicobasal membrane domains.