Metagenomic methods amplifying 16S ribosomal RNA genes have been used to describe the microbial diversity of healthy skin (HS) and lesion stages of bovine digital dermatitis (DD) and to detect critical pathogens involved with disease pathogenesis. In this study, we characterized the microbiome and for the first time, the composition of functional genes of HS, active (ADD) and inactive (IDD) lesion stages using a whole-genome shotgun approach. A total of 16 biopsy samples (HS, n = 8; ADD, n = 4; IDD, n = 4) were collected from Holstein dairy cows housed in one dairy farm. DNA was extracted and the microbiome was determined by shotgun techniques using Illumina MiSeq platform. Metagenomic sequences were annotated using MG-RAST pipeline. Six phyla were identified as the most abundant. Chordata, Firmicutes and Actinobacteria were the predominant phyla in the microbiome of HS, while Spirochetes, Bacteroidetes and Proteobacteria were highly abundant in ADD and IDD. T. denticola-like, T. vincentii-like and T. phagedenis-like constituted the most abundant species in ADD and IDD. Recruitment plots comparing sequences from HS, ADD and IDD samples to the genomes of specific Treponema spp., supported the presence of T. denticola and T. vincentii in ADD and IDD. Comparison of the functional composition of HS to ADD and IDD identified a significant difference (P < 0.05) in genes associated with motility/chemotaxis and iron acquisition/metabolism. We also provide evidence that the microbiome of ADD and IDD compared with that of HS had significantly higher (P < 0.05) abundance of genes associated with resistance to copper and zinc, which are commonly used in footbaths to prevent and control DD. In conclusion, the results from this study provide new insights into the HS, ADD and IDD microbiomes, improve our understanding of the disease pathogenesis and generate unprecedented knowledge regarding the functional genetic composition of the DD microbiome. Additionally, an increase in the abundance of copper and zinc resistance genes has been reported, suggesting that further research is necessary to optimize the foot bathing technique for the control and treatment of DD.