The recombination is one of the most frequently identified drivers of double-stranded DNA viruses evolution. However, the recombination events in African swine fever virus (ASFV) genomes have been poorly annotated. We hypothesize that the genetic determinants of ASFV variability are potential hot-spots for recombination. Here, we analyzed ASFV serotype-specific locus (C-type lectin (EP153R) and CD2v (EP402R)) in order to allocate the recombination breakpoints in these immunologically important proteins and reveal driving forces of virus evolution. The recombinations were found in both proteins, mostly among ASFV strains from East Africa, where multiple virus transmission cycles are notified. The recombination events were essentially associated with the domain organization of proteins. The phylogenetic analysis demonstrated the lack of clonal evolution for African strains which conclusively support the significance of recombinations in the serotype-specific locus. In addition, the signature of adaptive evolution of these two genes, pN/pS > 1, was demonstrated. These results have implications for the interpretation of cross-protection potential between evolutionary distant ASFV strains and strongly suggest that C-type lectin and CD2v may experience substantial selective pressure than previously thought.