Understanding how the expression of neuron class-specific genes is established during development is of key importance to the problem of neuronal diversity. Exploiting the molecular diversity of distinct motor neuron (MN) classes in C.elegans, we show that the evolutionarily conserved COE (Collier, Olf, Ebf) - type terminal selector UNC-3 is required for MN diversity by directly regulating the expression of MN class-specific terminal identity genes, such as ion channels and neurotransmitter receptors. We further find that Hox proteins cooperate with UNC-3 and remarkably employ two distinct, region-based strategies to generate MN diversity. In the C.elegans ventral nerve cord (VNC), the more anteriorly expressed Hox genes, lin-39/Scr/Dfd and mab-5 (Antennapedia-type), as well as the Hox cofactor ceh-20/Exd/Pbx are required for expression of MN class-specific terminal identity genes. Our mutational analysis shows that lin-39 and mab-5 – similarly to UNC-3 – directly activate MN class-specific genes, revealing a coactivation strategy that generates MN diversity along the VNC. Conversely, the posterior Hox gene egl-5/Abd-B acts as a repressor of lin-39 and mab-5 expression, thereby diversifying posteriorly located MN subclasses from their anterior homologs. Genetic removal of egl-5 results in homeotic transformation of posterior MN subclasses as evidenced by molecular and anatomical criteria. Intriguingly, we find that unc-3 and Hox orthologs are coexpressed in mouse MNs along the spinal cord, suggesting that this intersectional, region-based gene regulatory principle we uncovered in C.elegans may be conserved across phylogeny to generate neuronal diversity.