Dehalobacter is a genus of organohalide-respiring bacteria that is recognized for its fastidious growth using reductive dehalogenases (RDases). In the SC05 culture, however, a Dehalobacter population also mineralizes dichloromethane (DCM) produced by chloroform dechlorination using the mec cassette, just downstream of its active RDase. A closed genome of this DCM-mineralizing lineage has previously evaded assembly. Here, we present the genomes of two novel Dehalobacter strains, each of which was assembled from the metagenome of a distinct subculture from SC05. A pangenomic analysis of the Dehalobacter genus, including RDase synteny and phylogenomics, reveals at least five species of Dehalobacter based on average nucleotide identity, RDase and core gene synteny, as well as differential functional genes. An integration hotspot is also pinpointed in the Dehalobacter genome, in which many recombinase islands have accumulated. This nested recombinase island encodes the active RDase and mec cassette in both SC05 Dehalobacter genomes, indicating the transfer of key functional genes between species of Dehalobacter. Horizontal gene transfer between these two novel Dehalobacter strains has implications for the evolutionary history within the SC05 subcultures and of the Dehalobacter genus as a whole, especially regarding adaptation to anthropogenic chemicals.