Bovine Respiratory Disease (BRD) causes a severe form of pneumonia in all age of cattle. This study was designed to investigate the distribution of capsular types, serotypes, and virulence-associated genes of the major bacterial pathogens from BRD outbreak samples in Ethiopia. In this study 166 samples were collected from clinically sick (n = 107) and pneumonic lung tissue (n = 59). Laboratory assay confirmed isolation of M. haemolytica 37 (22.29%), P. multocida 25 (15.06%), B. trehalosi 12 (7.23%), and H. somni 15 (9.04%). PCR assay of P. multocida capsular typing revealed 21 (84.0%) cap A (hyaD-hyaC) and 4 (16.0%) cap D (dcbF) strains. M. haemolytica serotypes belonged to A: 1, A: 2, and A: 6 from 26 (70.27%), 4 (10.81%), and 7 (18.92%) isolates, respectively. P. multocida biotyping showed isolation of A: 1, A: 2, and A: 3 from 3 (14.29%), 2 (9.52%), and 16 (76.19%) isolates, respectively. M. haemolytica harbored more than 60% ssa gene, and 90.91% sodA while FbpA, TbpA, and lktC genes were found in all isolates. Likewise, all P. multocida exhibited toxA, FbpA, TbpA, and pmSLP genes. The current finding showed that M. haemolytica serotype A: 1 is frequently associated with BRD followed by P. multocida biotype A: 3. These two isolates harbored diverse virulence-associated genes and presented the pathogenic potential of the current isolates. Thus, investigation of pathogenic strains of BRD, virulence genes distribution, and molecular epidemiology of the disease from wider areas of the country are essential. Hence, continuous outbreak surveillance and molecular approaches are indispensable in designing efficient prevention strategies.