Molecular chaperones can prevent protein aggregation and assist proteins in reaching their structurally functional state. The molecular chaperone DNAJB6, a J-domain protein that partners with Hsp70s and nucleotide exchange factors, is very potent in preventing amyloid formation of proteins with large intrinsically disordered regions (IDRs), including several disease-associated proteins. Complementary to this, we recently demonstrated a role for DNAJB6 in surveilling IDP phase transitions, highlighting its role in nuclear pore complex assembly. Here, we further show that DNAJB6 and the closely related DNAJB2 and DNAJB8 prevent several FG-rich nucleoporins (FG-Nups) from undergoing aberrant phase-transitions. We demonstrate that this surveillance mechanism of DNAJB6 is encoded in an unusually highly conserved IDR that promotes the formation of stable, gel-like assemblies of the chaperone itself. These assemblies likely provide a stable environment that can outcompete homotypic FG-Nup interactions and instead favors dynamic, multivalent heterotypic chaperone:FG-Nup interactions. The evolutionary conservation of the DNAJB6-IDR and mutant analyses suggest that the sequence space for encoding stable gel-like assemblies is narrow and optimized to avoid self-aggregation while providing remarkable anti-amyloidogenic capacity.