Within proteins, intrinsically disordered regions (IDRs) are devoid of stable secondary and tertiary structures under physiological conditions and rather exist as dynamic ensembles of inter-converting conformers. Although ubiquitous in all domains of life, the intrinsic disorder content is highly variable in viral genomes. Over the years, functional annotations of disordered regions at the scale of the whole proteome have been conducted for several animal viruses. But to date, similar studies applied to plant viruses are still missing. Based on disorder prediction tools combined with annotation programs and evolutionary studies, we analyzed the intrinsic disorder content in Potyvirus, using a 10-species dataset representative of this genus diversity. In this paper, we revealed that: (i) the Potyvirus proteome displays high disorder content, (ii) disorder is conserved during Potyvirus evolution, suggesting a functional advantage of IDRs, (iii) IDRs evolve faster than ordered regions, and (iv) IDRs may be associated with major biological functions required for the Potyvirus cycle. Notably, the proteins P1, Coat protein (CP) and Viral genome-linked protein (VPg) display a high content of conserved disorder, enriched in specific motifs mimicking eukaryotic functional modules and suggesting strategies of host machinery hijacking. In these three proteins, IDRs are particularly conserved despite their high amino acid polymorphism, indicating a link to adaptive processes. Through this comprehensive study, we further investigate the biological relevance of intrinsic disorder in Potyvirus biology and we propose a functional annotation of potyviral proteome IDRs.