Migration and differentiation of cranial neural crest cells are largely controlled by environmental cues, whereas pathfinding at the trunk level is dictated by cell-autonomous molecular changes owing to early specification of the premigratory crest. Here, we investigated the migration and patterning of vagal neural crest cells. We show that (1) vagal neural crest cells exhibit some developmental bias, and (2) they take separate pathways to the heart and to the gut. Together these observations suggest that prior specification dictates initial pathway choice. However, when we challenged the vagal neural crest cells with different migratory environments, we observed that the behavior of the anterior vagal neural crest cells (somite-level 1–3) exhibit considerable migratory plasticity, whereas the posterior vagal neural crest cells (somite-level 5–7) are more restricted in their behavior. We conclude that the vagal neural crest is a transitional population that has evolved between the head and the trunk. Developmental Dynamics 240:2084–2100, 2011. © 2011 Wiley-Liss, Inc.