Abstract Remyelination, the biological process of restoring myelin sheaths, is critically dependent on the successful recruitment of oligodendrocyte lineage cells. However, this process involves at least two functionally distinct endogenous reservoirs: the widely distributed parenchymal oligodendrocyte precursor cells (pOPCs) and neural stem cells (NSCs) originating from the subventricular zone (SVZ). Emerging evidence reveals that these populations employ different migratory strategies. The pOPC response is characterized by rapid local proliferation but severely constrained, short-range migration, often limited by an inhibitory lesion microenvironment. In contrast, SVZ-derived precursors, including fate-switching neuroblasts, are capable of long-range, adaptive migrations, navigating complex routes by co-opting both vascular and parenchymal scaffolds. This review synthesizes these divergent phenomena into a unifying model of competing migratory programmes. We posit that the success or failure of endogenous repair depends on a dynamic interplay between the limited local pOPC response and the recruitment of the more plastic, long-range SVZ-derived cohort. We examine how the oligovascular niche and pivotal signalling cascades, including Wingless/Int-1–β-catenin (Wnt/β-catenin), bone morphogenetic protein (BMP), and sonic hedgehog/glioma-associated oncogene (Shh/Gli), function as critical regulators in this process, dictating which migratory strategy predominates in a given pathological context. Viewing remyelination as a dynamic balance between these two cellular systems helps explain why this repair process often fails. Ultimately, understanding these migratory programmes as an interconnected system, rather than as isolated components, is essential for developing more effective interventions that promote functional myelin repair in demyelinating diseases.