Lymphatic vessels are known to be derived from veins; however, recent lineage‐tracing experiments propose that specific lymphatic networks may originate from both venous and non‐venous sources. Despite this, direct evidence of a non‐venous lymphatic progenitor is missing. Here, we show that the zebrafish facial lymphatic network is derived from three distinct progenitor populations that add sequentially to the developing facial lymphatic through a relay‐like mechanism. We show that while two facial lymphatic progenitor populations are venous in origin, the third population, termed the ventral aorta lymphangioblast (VA‐L), does not sprout from a vessel; instead, it arises from a migratory angioblast cell near the ventral aorta that initially lacks both venous and lymphatic markers, and contributes to the facial lymphatics and the hypobranchial artery. We propose that sequential addition of venous and non‐venous progenitors allows the facial lymphatics to form in an area that is relatively devoid of veins. Overall, this study provides conclusive, live imaging‐based evidence of a non‐venous lymphatic progenitor and demonstrates that the origin and development of lymphatic vessels is context‐dependent. Synopsis The zebrafish facial lymphatics have three progenitor populations; one of these is non‐venous in origin and arises from a late‐forming angioblast population. This is the first time a non‐venous lymphatic progenitor has been described using live cell imaging. The zebrafish facial lymphatics form through the sequential addition of three progenitor populations in a relay mechanism. One of these progenitor populations, called the ventral aorta lymphangioblast (VA‐L), does not arise from a blood vessel, instead it arises directly from an angioblast population near the ventral aorta (VA‐A). The dorsal segment of the VA‐A expresses Prox1 and contributes towards facial lymphatic development while the ventral segment contributes to the hypobranchial artery. The zebrafish facial lymphatics have three progenitor populations; one of these is non‐venous in origin and arises from a late‐forming angioblast population. This is the first time a non‐venous lymphatic progenitor has been described using live cell imaging.