Fluoroquinolone-resistant extraintestinal pathogenic Escherichia coli (FQ-R ExPEC) assigned previously to phylogenetic group D were recently isolated from Australian dogs. This study aimed to better define the role of canine faeces as a reservoir of ExPEC clonal lineages of public health significance and their potential as canine pathogens. Sixty-seven fluoroquinolone-resistant E. coli isolates obtained from either the faeces of hospitalised dogs (n = 28) or canine extraintestinal infections (n = 39) were characterised and compared. Phylogenetic group was reassigned using the new Clermont multiplex PCR method and isolates underwent random amplified polymorphic DNA (RAPD) analysis, virulence genotyping, resistance phenotyping/genotyping, screening for human-associated ExPEC O-types, and multi-locus sequence typing. Canine faeces were identified to contain several sequence types (STs) also associated with clinical extraintestinal infections. These included ST354 (phylogroup F; 62.7%; 26 clinical, 16 faecal), ST420 (phylogroup B2, 1.5% 1 clinical); O1-ST38 (phylogroup D; 19.4%; 4 clinical, 9 faecal), O15:K52:H1-ST393 (phylogroup D; 4.5%; 1 clinical, 2 faecal), and O15:K1-ST130 (phylogroup D; 1.5%, 1 clinical isolate), O7-ST457 (phylogroup F; 3.0%; 1 clinical, 1 faecal) and O1-ST648 (phylogroup F; 3.0%; 2 clinical). RAPD profile-based analysis indicated three major clusters and 11 sub-clusters, whilst most ST-specific sub-clusters contained only faecal or clinical isolates, three (corresponding with ST354, ST393, and ST457) contained closely related, intermingled isolates from each source. All faecal isolates and 97% of clinical isolates exhibited a multidrug-resistant phenotype (MDR: resistant ≥ 3 antimicrobial classes) suggesting fluoroquinolone resistance as an indicator of MDR status. Median resistance scores did not differ significantly by source (median 4: P > 0.10). Genes encoding CTX-M and AmpC β-lactamases were identified in isolates from five of the seven STs. Overall, canine faeces are a large, previously overlooked reservoir of FQ-R-ExPEC clonal lineages, suggesting frequent zooanthroponotic transmission of FQ-R ExPEC between humans and dogs, possibly within both veterinary hospital and household environments.