Collective cell migrations are a major means by which animals' epithelial tissues move, reorganize, and remodel their environment. Epithelial cells are tightly adhered to one another in a continuous tissue sheet, so for a cell in the interior to move it must displace a neighboring cell. In this confined context, cells and their neighbors must coordinate their motility behaviors to move in concert rather than pushing and pulling one another unproductively. However, we have limited examples of the cellular and molecular mechanisms underpinning that coordination and do not know if they are generalizable. The follicular epithelium of Drosophila melanogaster offers an opportunity to test the generality of these mechanisms in vivo and to identify new ones. Follicle cells undergo a highly persistent collective migration that can be observed live with subcellular resolution as it occurs in an intact tissue and with its physiological substrate. This migration is made possible by an unconventional planar signaling system that couples the trailing edge of each cell to the leading edge of the cell behind. Several proteins in this system---Fat2, Lar, Sema5c, and Plexin A---have been identified. However, they have primarily been studied as discrete Fat2-Lar and Sema5c-Plexin A pairs, and the mechanisms by which they become planar-polarized and polarize the cells’ motility machinery are still largely unknown. I investigated how molecular interactions within and between these protein pairs maintain their polarized distributions, and how they work together to regulate the cells’ motility machinery, with a focus on their lamellipodia. I have organized my work into three data chapters (Chapters 2-4). In Chapter 2, I show that trailing edge-enriched Fat2 acts in trans to polarize the protrusive activity of the following cell, and that it accomplishes this by concentrating the lamellipoda-templating WAVE complex in puncta just across the interface from Fat2-containing puncta. In Chapter 3, I expand my focus to include Lar and Sema5c. Fat2 was previously shown to localize Lar in trans to leading edges, and I show that it does the same for Sema5c. From there, Lar and Sema5c signal in parallel to regulate migration. Fat2 therefore polarizes two arms of a planar signaling system, one including Lar and the other Sema5c and Plexin A, each with distinct outputs to the cell motility machinery. Previous phenotypic data and my own findings support a model in which Lar acts as an attractive cue by regulating protrusion at leading edges, and Sema5c and Plexin A signal repulsively to trailing edges. In Chapter 4, I present a new method for acutely inhibiting Fat2 and inducing disassembly of the Fat2-based puncta, and show that it can be used to follow puncta reassembly and the onset of collective migration ex vivo. Altogether, I find that Fat2 polarizes and aligns follicle cells' motility machinery using a multi-output planar signaling system with attractive and repulsive signaling arms. My work demonstrates how coordination strategies can be deployed combinatorially to give rise to emergent collective behaviors. It also highlights the overlapping challenges that tissues must overcome to achieve planar cell polarity and collective cell migration.