Burkholderia cenocepacia is an opportunistic pathogen within the Burkholderia cepacia complex (Bcc) which is rarely sourced from the environment and posses a severe risk for people with cystic fibrosis (pwCF). The recent classification of B. cenocepacia recA IIIB lineage isolates as a novel species, Burkholderia orbicola, with close genomic boundaries with B. cenocepacia raises concerns of the taxonomic accuracy of public genomic repositories and previous studies comparing environmentally and clinically derived isolates. In this collaborative study with the University of Mysore, India, we identified and taxonomically confirmed seven B. cenocepacia from the rhizosphere of medicinal plants. We reconstructed a comprehensive B. cenocepacia and B. orbicola genome collection by applying stringent quality control and bacterial taxonomic assignment through average nucleotide identity (ANI). Of the high-quality genomes (n=748), we identified that over one-third (37.6%; n=281) were misclassified, with B. orbicola (32.8%; n=246) mislabelled as B. cenocepacia. With focus on the true B. cenocepacia (n=467), we investigated population biology and performed a genome-wide association study to identify distinct genomic regions associated with environmental and CF sourced isolates. Through GWAS analysis a ~5000 bp region of chromosome 2 was identified as associated with CF-derived isolates. Sequence types identified within the collection corresponded to epidemic B. cenocepacia lineages, with ST33 and ST210 enriched in metal resistance genes. This study advances our understanding of B. cenocepacia by highlighting an environmental source of the species, its misclassification within the genomic databases and uncovering genomic traits associated with its environmental bacterium and high-risk CF pathogen phenotype.