The primary olfactory nervous system is unique in that it continuously renews itself and regenerates after injury. These properties are attributed to the presence of olfactory glia, termed olfactory ensheathing cells (OECs). Evidence is now emerging that individual OEC populations exist with distinct anatomical localisations and physiological properties, but their differential roles have not been determined. Unlike other glia, OECs can migrate from the periphery into the central nervous system, and organised OEC migration can enhance axonal extension after injury. Despite this, the mechanisms regulating OEC migration are largely unknown. Here, we provide an overview of the roles of OECs in development and adulthood. We review the latest research describing the differences between individual OEC subpopulations and discuss potential regulatory mechanisms for OEC guidance and migration. Using advanced time lapse techniques, we have obtained novel insights into how OECs behave in a complex multicellular environment which we discuss here with particular focus on cell-cell interactions. Significantly, transplantation of OECs constitutes a promising novel therapy for nerve injuries, but results are highly variable and the method needs improvement. We here review the roles of transplanted OECs in neural repair of damaged neuronal tracts distinct from the primary olfactory nervous system.