Underlying molecular mechanisms for the adaptive evolution of multidrug-resistant (MDR) pathogens have been poorly explored in both in vitro and in vivo conditions without antibiotic pressure. Recent multiomics-based techniques could be applicable for understanding how bacterial genomes have evolved to cope with nutritional stresses in environments. Genomics of laboratory-evolved MDR-A. baumannii NCCP 16007 (WT) cells serially subcultured for 8,000 generations under starvation (EAB1) or nutrient-rich (EAB2) conditions revealed the occurrence of large-scale of the genomic rearrangement, gene losses, and gains of insertion sequence (IS) elements. Transcriptomics and real-time qRT-PCR were conducted to demonstrate that altered expressions of many genes involved in growth rates (e.g, argG, rocC, gabD ), biofilm formation (e.g, ata, bamE, bap), and stress responses (e.g, katE, aqpZ, ydaD) contributed to corresponding phenotypes possibly by the aforementioned genomic changes. Surprisingly, thirty antibiotic resistance (AR) genes of different classes remained in the evolved genomes without significant changes in their gene expression and lipid A modification, suggesting that the stabilities of AR genes are stronger than expected during our evolution periods. Sudden changes of several tested phenotypes (growth rate, biofilm, polymyxin B resistance, and zeta potential) capabilities were substantially consistent with the presence or the absence of distinct regions in the genomes of the evolved cells recovered from different generation time points. Nutritional stress-driven genomic plasticities of A. baumannii cells mostly by the ISAba1 elements led to the modulation of many gene expressions, resulting in distinct phenotype traits for the survival of cells in hostile environments.