Bordetella bronchiseptica is a respiratory pathogen of humans and animals that infects a wide range of hosts. This study aimed to characterize the phylogenetic position and genomic features of 31 laboratory isolates of B. bronchiseptica, 25 of which were obtained from humans and six from animals. The studied isolates were compared with 30 reference genomes of B. bronchiseptica, B. pertussis, and B. parapertussis. The analysis included the determination of average nucleotide identity (ANI), phylogenetic reconstruction based on 120 marker proteins and 42 ribosomal proteins, and the identification of virulence factors, potential antibiotic resistance genes, prophage regions, and antiphage defense systems. A subsample of 20 genomes has also been subjected to pangenomic and metabolic analyses. In the overall dataset, B. pertussis and B. parapertussis formed compact clades, whereas B. bronchiseptica isolates were distributed across several phylogenetic lineages. B. bronchiseptica lines differed in their repertoires of virulence factors, putative antibiotic-resistance determinants, prophages, and antiphage defense systems. In the subsample of 20 genomes, representatives of the classical Bordetella retained the main modules of central metabolism and a substantial proportion of the shared gene clusters. The resulting data demonstrate a pronounced phylogenetic and functional genomic heterogeneity of B. bronchiseptica.