The global dissemination of fluoroquinolone-resistant (FQr) extra-intestinal pathogenic Escherichia coli (ExPEC) poses an increasing challenge for the management of ExPEC infections. Among the FQr ExPEC, sequence type (ST)1193 is the second most common globally disseminated lineage (after ST131), however, little is known about its evolution. Here, we present the first comprehensive genomic analysis of this emerging FQr ExPEC lineage. Using whole-genome sequencing (WGS), we undertook genomic analyses of a national collection of 55 Australian ST1193 isolates (53 human, 2 domesticated canines), spanning 2010–2013. All isolates were subjected to WGS-based in silico serotyping against E. coli specific O-antigen, H-antigen, and K-antigen databases. Fimbrial-typing categorised fimH alleles. A high-resolution phylogeny was built using core-genome single nucleotide polymorphisms (SNPs) with an additional 221 publicly available global ST1193 assemblies. Antimicrobial resistance (AMR) gene presence was determined by nucleotide comparisons of draft assemblies against AMR databases. FQr-associated SNPs in gyrA and parC were detected using read-mapping. The ST1193 lineage falls within phylogenetic group B2, which is predominantly associated with ExPEC. The O75:H5-ST1193 lineage contains a range of ExPEC-associated virulence determinants (e.g. fimbriae and toxin encoding genes) and clusters into two clades distinguishable by K1/K5 capsular antigens. All ST1193 isolates have the fimH64 allele. The canine isolates clustered closely with human isolates, suggesting possible transmission between humans and companion animals. No geographical clustering was observed. FQr-associated SNPs in gyrA (S83L and D87N), and parC (S80I) were detected across all ST1193 isolates. Additionally, four CTX-M extended-spectrum beta-lactamases (ESBL) resistance alleles, including blaCTX-M-15, were detected among several O75:H5:K1-ST1193 isolates but none of the O75:H5:K5-ST1193 isolates. This is the first comprehensive in silico analysis of the O75:H5-ST1193 clonal lineage. Here, we characterise a rapidly emerging, highly resistant ExPEC lineage and establish a genomic framework for future investigations into this important human pathogen.