Wnt signaling and HOM-C/Hox genes pattern cell fate along the anterior/posterior axis in many animals. In general, Wnt signaling participates in establishing the anterior/posterior axis, whereas HOM-C genes confer regional identities to cells along the axis. However, recent work in non-bilaterial metazoans suggests that the ancestral patterning system relied on Wnts, with a later co-option of HOM-C genes to replace Wnts in regional patterning. Here we provide direct experimental support for this model from C. elegans, where a regional Wnt patterning system is uncovered in HOM-C gene mutants. Anterior/posterior patterning of P11/P12 cell fate in the C. elegans tail is normally dependent on the HOM-C gene egl-5/Abdominal-B. If the HOM-C gene mab-5/fushi tarazu is also mutant, however, a Wnt signal can promote P12 fate in the absence of egl-5. Furthermore, transcription of egl-5 in the P12.pa cell is influenced by an autoregulatory element that is essential in wild type, but not in mab-5 egl-5 double mutants, identifying regulatory parallels between P12 cell fate specification and egl-5 transcriptional regulation in the P12 lineage. Together, our results identify complex regulatory relationships among signaling pathways and HOM-C genes, and uncover a layering of patterning systems that may reflect their evolutionary history.