Abstract text: The β-1,4-linked mannans are the most ancient hemicellulosic polymers in plant cell walls and serve as versatile hydrocolloids that define plant biology and support diverse industrial applications, including food and medicine. Despite their importance, the biological function and evolutionary origin of these polysaccharides remain unknown, limiting our ability to tailor their structure in crops and microbial cell factories. Porphyra umbilicalis is an ancient red alga where crystalline mannan replaces cellulose as the load-bearing polysaccharide. Utilizing synthetic yeast and plant chassis, we demonstrate that P. umbilicalis CELLULOSE SYNTHASE-LIKE K1 (PumCSLSK1) encodes an ancient mannan synthase that predates terrestrial plant CSLA. PumCSLK1 localized to intercellular puncta in yeast and produced pure mannan that altered cell wall properties. In planta, overexpression of PumCSLK1 in the seed coat perturbed cell morphology, despite other CSLA/Ks homologs enhancing mannan accumulation and maintaining seed coat structure. Collectively, our findings identify PumCSLK1 as a Golgi-localized ancestral mannan synthase, illuminating the early evolution of mannan biosynthesis. This work highlights the diverse and complex nature of mannans and establishes a fundamental framework for engineering their production and structural design in crops and synthetic biological systems.