Canine circovirus (CanineCV) is a deadly pathogen affecting both domestic and wild carnivores including dogs. No vaccine against CanineCV is available commercially or under clinical trials. In the present study, we have designed a promising multiepitope vaccine (MEV) construct targeting multiple strains of CanineCV. A total of 545 MHCII binding CD4+T cell epitope peptides were predicted from the capsid and replicase protein from each strain of CanineCV. Five conserved epitope peptides among the three CanineCV strains were selected. The final vaccine was constructed using antigenic, nontoxic, and conserved multiple epitopes identified in silico. Further, molecular docking and molecular dynamics simulations predicted stable interactions between the predicted MEV and canine receptor TLR-5. To validate antigenicity and immunogenicity, one of the mapped epitope peptides was synthesized. In vivo analysis of the selected epitope clearly indicates CD4+T-cell-dependent generation of antibodies which further suggests that the designed MEV construct holds promise as a candidate for vaccine against CanineCV.