The unified genotypic classification scheme (genotypes A0, A1–A8, and B1–B5) was proposed and applied for the classification of the infectious bursal disease virus (IBDV). Since 1987, IBDVs have circulated and evolved in Vietnam, but little is known about the genotypes present. The IBDV samples were collected in 1987, 2001–2006, 2008, 2011, 2015–2019, and 2021 in 18 provinces. We conducted phylogenotyping analysis based on the alignment of 143 VP2-HVR (439 bp, nt 628–1066; aa 210–355 in VP2), including 64 Vietnamese isolates and two vaccines, and 82 VP1 B-marker (725 bp, nt 13–737; aa 4–245 in VP1) sequences, including four Vietnamese isolates and one vaccine. The analysis revealed three A-genotypes, A1, A3, and A7, and two B-genotypes, B1 and B3, among the Vietnamese IBDVs. The IBDV strains showed the lowest average evolutionary distance at 8.6% between A1 and A3 and the highest (21.7%) between A5 and A7, while 14% was between B1 and B3 and 17% between B3 and B2. The signature residues 222T - 253Q - 256V - 294L - 299(S/N) appeared to be unique for the genotype A2; the 222A - 253Q - 256I - 294I - 299S for the A3, the 222T - 253Q - 256V - 294L - 299N for the A5, the 222Q - 253E - 256K - 294L - 299S for the A6, and the 222A - 253Q - 256A - 294L - 299S for the A8, and each of these could be the genotypical motif for genotypic discrimination. The timeline statistical summary revealed that the A3-genotype predominated (79.8% presence) in Vietnam from 1987 to 2021 and that it has remained dominant in circulating IBDVs over the last five years (2016–2021).