Organisms across all kingdoms of life utilize intrinsically disordered proteins (IDPs) as a strategy for desiccation tolerance. Studying the sequence features of known desiccation-related IDPs can provide insights into their mechanistic similarities in achieving this function. A distinctive family of IDPs specific to tardigrades is the cytoplasmic abundant heat-soluble (CAHS) proteins. Despite the differences in sequence and conserved domains, many desiccation-related IDPs share similarities in gaining helical secondary structures upon drying, leading to the hypothesis that the structural transition of IDPs is linked to their protective capacity. In addition to adopting a helical secondary structure, many IDPs oligomerize in response to a drying-induced increase in concentration, suggesting that oligomerization is a crucial mechanism of desiccation tolerance. However, empirical evidence regarding the role of structural transition in desiccation protection is lacking, as is an understanding of how IDP oligomerization promotes desiccation protection. CAHS D, a model CAHS protein, exhibits a helical propensity that increases upon drying, concentration-dependent gelation, and robust desiccation protective capacity, making it an ideal IDP for testing these speculated mechanisms of desiccation tolerance. Using CAHS D, we demonstrate that the helical linker region of this protein drives robust client enzyme protection during drying. However, helicity alone does not determine desiccation tolerance. Instead, the linker amphipathic helix promotes antiparallel dimer formation, a crucial step in the oligomerization to the higher-order assembly of CAHS D gelation, promoting desiccation protection. Beyond illustrating the sequence features of CAHS D helicity and oligomerization, this work sheds light on desiccation-related IDPs with similar sequences and structural features and provides insights for developing dry preservation technologies.