Bluetongue (BT) is a severe arboviral disease affecting sheep, cows, and other wild ruminants, caused by the Bluetongue virus (BTV). The virus has evolved into over 32 serotypes, rendering existing vaccines less effective. While the structural proteins of this virus represent promising targets for vaccine development, they unfortunately exhibit high amino acid polymorphism and are laden with numerous inhibitory epitopes. However, certain structural proteins such as VP1 and VP7 are highly conserved and may contain epitopes capable of triggering cross-reactive cell-mediated immunity (CMI). In this study, we identified highly conserved MHC-I and -II-restricted T cell epitopes within VP1, VP5, and VP7 BTV proteins and developed an effective in silico-immuno-informatics-based broad-spectrum BT multiepitope vaccine for laboratory mouse system to establish a proof-of-concept, as well as for bovines, the natural host for BTV. The conserved epitopes utilized in the vaccines are highly antigenic, non-allergenic, non-toxic, and predicted to be capable of inducing IFN-𝛾. Both mouse and bovine vaccines were tethered with Toll-like receptor (TLR)-4-agonist adjuvants, beta-defensin 2 or 50S ribosomal unit to stimulate innate immunity for CMI development. Protein-protein docking analysis revealed strong binding affinities, while extensive 100-nanosecond molecular dynamics simulations indicated stable complexes between the vaccine structures and TLR4. These novel vaccine designs address an urgent clinical need in the livestock industry by potentially preventing and controlling BT in ruminants, warranting further exploration and validation through experimental studies.