In eukaryotic cells, heat shock and other stresses trigger the accumulation of proteins and RNA into cytosolic ribonucleoprotein (RNP) stress granules marked by poly(A)-binding protein. Formation of stress granules is thought to be an adaptive response involved in global regulation of translation, yet these ideas have been difficult to test given the lack of mutational perturbations linking protein behavior to phenotype. Stress granule formation has been reported to involve multivalent RNA/protein and protein-protein interactions such as those mediated by intrinsically disordered regions (IDRs) whose molecular evolution remains enigmatic. Here we report that poly(A)-binding protein itself, Pab1 in yeast, autonomously forms heat-induced RNP granules in vitro. Pab1’s highly conserved IDR, the proline-rich “P domain”, modulates but is not essential for the formation of heat-induced RNP granule assembly in vivo and in vitro. Evolutionary analysis of the P domain reveals previously unappreciated patterns of selection on its composition, particularly its aliphatic residues. We show experimentally that these residues tune the IDR’s conformational and biological properties including collapse of the domain, heat-induced Pab1 granule formation in vivo and in vitro, and yeast thermotolerance. Although heat-induced protein aggregation is generally thought to be harmful, we discover that mutations that reduce Pab1’s heat-triggered aggregation also reduce cells’ ability to grow at elevated temperatures. Pab1's role as a translational regulator appears tightly linked to its stress-triggered self-assembly. Our results indicate that poly(A)-binding protein’s heat-induced aggregation represents a largely autonomous, evolutionarily tuned, adaptive self-assembly response to stress.