The spread of carbapenemase-producing
Enterobacterales
(CPE) is of major public health concern. The transmission dynamics of CPE in hospitals, particularly at the national level, are not well understood. Here, we describe a retrospective nationwide genomic surveillance study of CPE in Ireland between 2012 and 2017. We sequenced 746 national surveillance CPE samples obtained between 2012 and 2017. After clustering the sequences, we used thresholds based on pairwise SNPs, and reported within–host diversity along with epidemiological data to infer recent putative transmissions. All clusters in circulating clones, derived from high-resolution phylogenies, of a species (
Klebsiella pneumoniae
,
Escherichia coli
,
Klebsiella oxytoca
,
Enterobacter cloacae
,
Enterobacter hormaechei
and
Citrobacter freundii
) were individually examined for evidence of transmission. Antimicrobial resistance trends over time were also assessed. We identified 352 putative transmission events in six species including widespread and frequent transmissions in three species. We detected putative outbreaks in 4/6 species with three hospitals experiencing prolonged outbreaks. The bla
OXA-48 gene was the main cause of carbapenem resistance in Ireland in almost all species. An expansion in the number of sequence types carrying bla
OXA-48 was an additional cause of the increasing prevalence of carbapenemase-producing
K. pneumoniae
and
E. coli
.