Cells organize their contents and regulate cell shape and mechanics through molecular motors functioning on cytoskeletal filaments. Myosin X, an actin-based motor that concentrates at the distal tips of filopodia of mammalian cells, 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. Recently we showed that the post-IQ region is the main contributor to myosin X's selectivity. This region contains a charged single alpha-helix (SAH), which may impart unique mechanical or affinity properties to the motor. The structural character of this region was perturbed by insertion of a free swivel (GSGGSG flexible linker) after the SAH domain. The post-SAH swivel mutant showed no preference for bundled actin for motility in vitro, 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. Here we investigate if interrupting the “selectivity module” also has the described effect in live cells.We overexpressed in the U2OS cell line three fluorescently tagged forms of myosin X: the GCN4 forced dimer used in in vivo experiments, the post-SAH swivel mutant of GCN4 dimer and the wild type with a native dimerization domain. GCN4 forced dimer performs in the cell in the same manner as full- length myosin X. Introducing a free swivel in the SAH domain region affects the selective nature of myosin X in the natural cytoskeleton environment of the cell interior as co-localization of GFP labeled protein with filopodial tips does not occur for the Swivel mutant.