Despite decades of research since the discovery of the environmental sensitivity of tropoelastin, only a handful of elastin-inspired polypeptides departing from the canonical VPGXG motif, where X is any amino acid except proline, have been uncovered. Hence, the field of "smart" protein-polymers has evolved mainly through the introduction of innovative molecular architectures. Instead, we decided to explore sequence diversity as a necessary tool to broaden the biomedical and biotechnological utility of these "smart" protein-polymers. Using a new, highly parallel method for the synthesis of repetitive genes, we conducted a systematic study of the sequence constraints of the canonical VPGXG motif by substituting or inserting Alanine residues along this pentapeptide motif, which yielded new pentapeptide and hexapeptide, non-canonical ELP motifs. These studies led to the discovery of new families of hexapeptide motifs with fully reversible phase transition behavior and suggested an unexpected degree of sequence and conformational promiscuity in the canonical motif that hints at the existence a large space of amino acid sequences with intrinsic "smart" behavior. Moreover, this work shed light into the conformational requirements of the phase transition behavior and suggested the possibility to control the assembly of "smart" protein-polymers in a sequence-controlled manner.