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A central goal in developmental biology is to decipher the molecular events that govern cell fate specification in each developmental lineage. Here, we show that the C. elegans Forkhead transcription factor UNC-130 specifies two glial types that arise from one lineage, but does not affect equivalent glia that are produced in different anatomical regions from other lineages. We show that glial defects correlate with UNC-130:DNA binding, and that UNC-130 acts as a transcriptional repressor via two independent domains. UNC-130 can be functionally replaced by its human homolog, the neural crest lineage determinant FoxD3, and other neural crest factors (UNC-86/Brn3 and RNT-1/Runx) act in the same pathway. We propose that, in contrast to “terminal selectors”, UNC-130 acts as a "lineage selector" to enable molecularly distinct progenitor cells to generate regionally equivalent cell types. This novel mechanism may underlie the recent observation of convergent lineages as a prevalent feature of vertebrate development.