While directed cellular migration facilitates the coordinated movement of cells throughout development, in wound repair, and during an immune response, the precise mechanisms regulating such migration in vivo remain inadequately understood. Missing in Metastasis (MIM) is a defining member of the I-BAR subfamily of lipid binding, actin cytoskeletal regulators whose levels are altered in a number of cancers. Here I provide the first genetic evidence that I-BAR proteins regulate directed cell migration in vivo. MIM regulates the directional migration of several cell types responding to a number of different guidance cues. While regulating the directionality of migrating cells has been demonstrated in vitro, this role of an I-BAR protein in vivo was not previously observed. I demonstrate in these studies that Drosophila MIM (DMIM) is required for border cell migration, with loss of dmim function resulting in a lack of directional movement by the border cell cluster. In vivo endocytosis assays combined with genetic analyses demonstrate that the dmim product regulates directed cell movement by inhibiting endocytosis and antagonizing the activities of the endophilin/CD2AP/cortactin complex in these cells. These studies demonstrate that competition between BAR family members for pro-endocytic components underlies a directional sensing mechanism during guided cell migration.