Klebsiella oxytoca is an emerging pathogen that can cause life-threatening infectious diseases in humans. Recently, we firstly reported for the first time the presence of K. oxytoca in edible aquatic animals. In this study, we further investigated its bacterial environmental fitness and genome evolution signatures. The results revealed that K. oxytoca isolates (n = 8), originating from eight species of aquatic animals, were capable of growing under a broad spectrum of environmental conditions (pH 4.5–8.5, 0.5–6.5% NaCl), with different biofilm formation and swimming mobility profiles. The genome sequences of the K. oxytoca isolates were determined (5.84–6.02 Mb, 55.07–56.06% GC content). Strikingly, numerous putative mobile genetic elements (MGEs), particularly genomic islands (GIs, n = 105) and prophages (n = 24), were found in the K. oxytoca genomes, which provided the bacterium with specific adaptation traits, such as resistance, virulence, and material metabolism. Interestingly, the identified prophage-related clusters were derived from Burkholderia spp., Enterobacter spp., Klebsiella spp., Pseudomonas spp., and Haemophilus spp., suggesting phage transmission across Klebsiella and the other four genera. Many strain-specific (n = 10–447) genes were present in the K. oxytoca genomes, whereas the CRISPR-Cas protein-encoding gene was absent, indicating likely active horizontal gene transfer (HGT) and considerable genome variation in K. oxytoca evolution. Overall, the results of this study are the first to demonstrate the environmental compatibility and genome flexibility of K. oxytoca of aquatic animal origins.