Localization and local translation of oskar mRNA at the posterior pole of the Drosophila oocyte directs abdominal patterning and germline formation in the embryo. The process requires precise recruitment and regulation of motor proteins to form transport-competent mRNPs. Using high- and super-resolution imaging, we determine the steps in motor recruitment to oskar mRNPs. We show that the posterior-targeting kinesin-1 is recruited upon nuclear export of oskar mRNPs, prior to their dynein-dependent transport from the nurse cells into the oocyte. We demonstrate that DmTropomyosin1-I/C is an atypical RNA-binding, nucleocytoplasmic shuttling Tropomyosin1 isoform that binds the oskar 3′UTR through recognition of a supramolecular RNA motif created upon dimerization of oskar molecules. Our data show that, in the oocyte, kinesin-1 is recruited by DmTropomyosin1-I/C to a dynamically changing, small subset of oskar mRNPs and is activated by the functionalized spliced oskar RNA localization element, revealing an ergonomic, coordinated mechanism of cargo transport.