bla_CMY-2 is the most prevalent plasmid-borne AmpC β-lactamase gene in Escherichia coli globally and confers resistance to cephalosporins and β-lactamase inhibitors. bla_CMY-2 was captured from the chromosome of Citrobacter freundii by ISEcp1 and is invariably found with this insertion sequence in a variety of different genetic contexts and plasmid lineages. IncI1 plasmids appear to be important in the transmission of bla_CMY-2 among E. coli populations, including in Australia. We previously sequenced an IncI1 plasmid from Sydney and identified a novel bla_CMY-2 context in which ISEcp1 is truncated by IS1294, leaving only 161 bp. A 159-bp fragment of IncA/C plasmid backbone downstream of bla_CMY-2 suggests mobilisation from an IncA/C plasmid by IS1294. A 2.3 kb region adjacent to the right end of IS1294 was missing compared to other IncI1 plasmids. PCR identified plasmids with similar insertions in over 40 diverse E. coli isolated in Sydney over a number of years. Sequencing of a subset of these isolates with Illumina MiSeq technology identified related IncI1 plasmids that do not have a deletion adjacent to IS1294, as well as examples of four different sized deletions. There were few differences across the backbones, except in regions related to entry exclusion and conjugal transfer that may represent functional differences. The unique bla_CMY-2 insertion and the similarities between these plasmids suggest that they originated from a common ancestor and subsequent diversification may have occurred via deletions and homologous recombination. Two almost identical plasmids (<10 SNPs) isolated from the same E. coli sequence type five years apart may indicate clonal spread of a bla_CMY-2-E. coli strain. The dissemination of bla_CMY-2 in Sydney thus appears to be multifactorial, involving clonal spread of E. coli strains and horizontal transfer of related, but not identical, IncI1 plasmids to diverse E. coli subtypes.