Cells organize their contents and regulate cell shape and mechanics through molecular motors functioning on cytoskeletal filaments. Presented with many apparently similar tracks within the cortex, how myosins identify the few actin filaments that lead to their correct cellular destinations is largely unknown. Myosin X, an actin-based motor that concentrates at the distal tips of filopodia, selects the fascin-actin bundle at the filopodial core for motility. While poorly processive on single actin filaments, it takes processive runs on actin bundled by fascin. Such a bundle is the precise structure to which myosin X localizes in vivo. Using single molecule optical trapping experiments we determined the step size to be 17 nm, half of the 36 nm pseudo-helical actin repeat essential for motors to be processive on single actin filaments. This suggested that straddling two filaments within a bundle stimulates this motor's processivity. Using combinatorial chimeric constructs of myosin V and myosin X, we show that the post-IQ region, not the short lever arm (three IQ repeats) or the motor domain, is the main contributor to myosin X's selectivity. This region contains two structures of interest: a charged single alpha-helix (SAH), which may impart unique mechanical or affinity properties to the motor, and a coiled-coil dimerization motif. The structural character of this region was perturbed by insertion of free swivels either before or after the SAH domain. The post-SAH swivel mutant showed no preference for bundled actin for motility, thus providing support to a selectivity model where the search-space of the forward head for the next binding site is constrained to neighboring filaments in a bundle. This result provides insight into the ability of nature to fine-tune myosin motors to serve their specific functions in the cell.