In vivo functions of the septin and actin cytoskeletons are closely intertwined, yet the mechanisms underlying septin-actin crosstalk have remained poorly understood. Here, we show that the yeast-bud-neck-associated Fes/CIP4 homology Bar-amphiphysin-Rvs (F-BAR) protein suppressor of yeast profilin 1 (Syp1)/FCHo uses its intrinsically disordered region (IDR) to directly bind and bundle filamentous actin (F-actin) and to physically link septins and F-actin. Interestingly, the only other F-BAR protein found at the neck during bud development, Hof1, has related activities and also potently inhibits the bud-neck-associated formin Bnr1. However, we find that Syp1 enhances rather than inhibits Bnr1-mediated actin assembly and fully overcomes Hof1-mediated inhibition of Bnr1. Further, during bud development, Syp1 and Hof1 show reciprocal patterns of arrival and departure from the bud neck, and in vitro Syp1 and Hof1 compete for septin binding. Together, our observations suggest that as the bud grows, the relative levels of these two F-BAR proteins at the bud neck invert, driving changes in septin organization, septin-actin linkage, and formin activity. More broadly, our findings expand the functional roles of Syp1/FCHo family proteins and our understanding of the working relationships among F-BAR proteins in cytoskeletal regulation.