The glia of the olfactory system, olfactory ensheathing cells (OECs) are excellent candidates for neural repair. In their natural environment within the olfactory system, OECs are present within the peripheral nervous system and the central nervous system and they are considered to be crucial to the ability of olfactory neurons to regenerate throughout life. However, OECs are not a uniform population. Instead there are different subpopulations, each with a different molecular profile and proposed role in vivo. If OECs are to be used for neural repair therapies, it is therefore important to consider the different characteristics of the various subpopulations of OECs and their potential therapeutic benefit. Using in vitro assays, we have determined that OECs derived from the peripheral nervous system in the nasal cavity respond differently to OECs isolated from the olfactory bulb in the central nervous system. Peripheral OECs are a uniform population that predominantly adhere to each and thereby promote contact-mediated migration of each other. In contrast, OECs from the olfactory bulb are a heterogeneous population that exhibit differential preference for contact with each other and are less likely to promote contact-mediated migration. We have further purified OECs from distinct anatomical regions of the olfactory bulb and used cell behaviour assays to reveal that OECs obtained from the rostral, ventral, dorsal and caudal regions of the olfactory bulb all exhibit strikingly different behaviours during cell-cell contact. The behaviours of the different subpopulations of OECs are consistent with their proposed roles in vivo. We found that the heterogeneity of the OECs is regulated by motile lamellipodial waves and that inhibition of the lamellipodial wave activity abolishes the ability of the cells to distinguish between each other. These results demonstrate that individual subpopulations of OECs with distinct properties exist within the olfactory nervous system. These results have important implications for selecting the source of OECs for neural transplant therapies.