$Klebsiella\; oxytoca$, a member of the Enterobacteriaceae, is a gram-negative pathogenic bacterium of environmental origin, which can cause infection in healthcare settings. Outbreaks of multidrug-resistant $K.\; oxytoca$ infection have been increasingly reported in hospitalized patients. Despite the growing importance of this pathogen, there is limited knowledge about the population structure and epidemiology of antimicrobial resistant $K.\; oxytoca$. We investigated the population structure and genomic basis of antimicrobial resistance of 41 multidrug resistant $K.\; oxytoca$ isolates recovered from bloodstream infections across the UK and Ireland. Our results show that $K.\; oxytoca$ has a highly diverse population, which is composed of several distinct clades, and we identified one recent expansion of a clone within our dataset. Although the $K.\; oxytoca$ genomes are clearly distinct from the genomes of a global collection of $Klebsiella\; pneumoniae$ complex, pre-dominantly composed of $K.\; pneumoniae$, we found evidence for sharing of core genes through recombination, as well as the exchange of accessory antimicrobial resistance and virulence factor genes between the species. Our findings also suggest that the different $K.\; oxytoca$ clades have acquired antimicrobial resistance and virulence factor genes independently. This highlights the clinical and therapeutic importance of genetic flexibility in $K.\; oxytoca$ and the relevance of this in its role as an opportunistic pathogen.