Avian avulaviruses (avulaviruses or AAvVs) infect a wide range of avian species worldwide with variable clinical outcomes and economic impacts. Owing to broad host spectrum, several novel avulaviruses are being reported from both wild and domesticate birds that highlight the potential of the virus to evolve, adapt and emerge in susceptible population. Pathobiological and phylogenetic characterizations of individual avulaviruses are often demonstrated, however, a cumulative and comparative assessment of avulaviruses remains elusive. To assess evolutionary dynamics and potential emergence of novel avulaviruses, we enriched existing databases of all known avulaviruses (specie-type 1-20), and determined their genomics features based on both complete genomes and individual complete genes. While a high nucleotide divergence (up to 65.4%) was observed among avulaviruses, phylogenomic analysis revealed clustering of all avulaviruses into three distinct clades. The major clade (Clade-I) included both oldest and newest avulaviruses (2, 5, 6, 7, 8, 10, 11, 14, 15 and 20) and the second clade (Clade-II) consisted of avulaviruses 1, 9, 12, 13, 16, 17, 18 and 19, whereas the third clade (Clade-III) carried only avulaviruses 3 and 4. Intriguingly, clustering pattern was descriptive for individual gene-based analysis, however, the hemagglutinin-neuraminidase (HN) and polymerase (L) genes showed clear and discrete branching patterns similar to complete genome-based clustering. Therefore, we propose the use of HN, or L genes or complete genome to study epidemiological aspects of the avulaviruses. Genomic and residue characteristics of all genes indicated a continuous evolution of the virus, and substitutions in biologically important motifs warrant future investigations to assess their roles in the pathobiology of the virus. Taken together, this comprehensive analysis of all known avulaviruses ascertains continuous monitoring and surveillance of wild/water-fowls and commercial poultry. These findings further our understanding on the evolutionary dynamics and potential emergence of novel avulaviruses and will establish bases to identify potential of wild-bird origin apathogenic viruses to cause infections in commercial poultry.