The gram-negative bacterium “Haemophilus parasuis” is the etiologic agent of Glässer’s disease in pigs, and causes significant economic losses to the swine industry. This bacterium is classified as a member of the family Pasteurellaceae in the genus Haemophilus based on its requirement for nicotinamide adenine dinucleotide (NAD) for growth. However, other phenotypic traits and phylogenetic relatedness have not been examined to support this genus classification, and therefore were the subject of this investigation. All 19 complete “H. parasuis” genomes plus those of representative Pasteurellaceae were subjected to phylogenetic analysis of multi-protein alignments. Based on this analysis the closest relative to “H. parasuis” among sequenced genomes is Bibersteinia. Sequencing of the 16S rDNA and the rpoB loci of the 15 serovar type strains of “H. parasuis” assigned these isolates to two clades within the species “H. parasuis”, but with little structure within these divisions, consistent with the genome-wide analysis by Howell et al. (BMC Genomics 2014, 15:1179). The metabolic phenotypes of 38 “H. parasuis” strains were determined and compared to other members of the Pasteurellaceae. All 38 strains of H. parasuis were positive for catalase activity, oxidase activity, V-factor requirement, Voges-Proskauer (acetoin) test, and acid formation from D-galactose and D-glucose. Acid formation from L-arabinose, D-mannose, maltose, sucrose, D-fructose, myo-inositol, and D-ribose was variable. All 38 strains were negative for X-factor requirement, indole production from tryptophan, and α-glucosidase and alkaline phosphatase activity. Our results place “H. parasuis” in a very distinct lineage from other bacteria labelled “Haemophilus”, warranting its assignment to a novel genus within the family Pasteurellaceae that we propose as Glaesserella parasuis gen. nov., comb. nov.