F-BAR proteins bind the plasma membrane (PM) to scaffold and organize the actin cytoskeleton. To understand how F-BAR proteins achieve their PM association， we studied the localization of a Schizosaccharomyces pombe F-BAR protein Rga7， which requires the coiled-coil protein Rng10 for targeting to the division site during cytokinesis. We find that the Rga7 F-BAR domain directly binds a motif in Rng10 simultaneously with the PM， and that an adjacent Rng10 motif independently binds the PM. Together， these multivalent interactions significantly enhance Rga7 F-BAR avidity for membranes at physiological protein concentrations， ensuring the division site localization of Rga7. Moreover， the requirement for the F-BAR domain in Rga7 localization and function in cytokinesis is bypassed by tethering an Rga7 construct lacking its F-BAR to Rng10， indicating that at least some F-BAR domains are necessary but not sufficient for PM targeting and are stably localized to specific cortical positions through adaptor proteins.