Acinetobacter is an important opportunistic pathogen associated with severe infections in humans and animals worldwide. In veterinary medicine, the resistance patterns of Acinetobacter species remain unclear, with limited information available. This study examined the genomics characterization and antimicrobial resistance of Acinetobacter strains from swine industry of Shanxi province in China. The analysis of core genome phylogenetic and antibiotic genetic determinants from Acinetobacter has shown that the number of specific core genes varied from 105 to 293, with TG9 as an outlier. Functional gene annotation from COG, GO, and KEGG analyses revealed high consistency, particularly in genes related to amino acid transport, metabolism, transcription, and energy production. Meanwhile, these strains exhibited the endemic characteristics of Acinetobacter spp., as well as the close evolutionary relationships of antibiotic resistance genes. All isolated strains had a high multidrug resistance (50%), which highlights their pathogenic for oxacillin (79.2%), cefazolin (41.7%), cotrimoxazole (50%), and tetracycline (25%). Upon treatment with ampicillin, cefotaxime, and sulfonamides, the expression of OXA51, AmpC, abeM, abeS, TEM, and sul2 mRNA in various specific Acinetobacter strains were elevated to different extents, particularly pronounced upregulation in A. baumannii. This study significantly advances our understanding of antibiotic resistance in foodborne Acinetobacter. It provides valuable theoretical insights for controlling the spread of Acinetobacter species and reducing the associated public health risks.