Burkholderia contaminans, a species of the Burkholderia cepacia complex—prevalent in certain Latin-American and European countries—can cause chronic pulmonary infection in persons with cystic fibrosis. Our aim was to gain insights into long-term lung infections with a focus on correlating how bacterial phenotypic traits in the chronic infection impact on patients´ clinical outcome. Genotypic characteristics of 85 B. contaminans isolates recovered from 70 patients were investigated. For 16 of those patients, the clinical status and bacterial phenotypic characteristics, e. g., several virulence factors, phenotypic variants, and the antimicrobial susceptibility pattern, were evaluated. Two clones were found in the whole bacterial population: i) the multiresistant ST 872 PCR-recA-RFLP-HaeIII-K–pattern clone which carries a pathogenic island homologous to BcenGI11 of B. cenocepacia J2315, and ii) the ST 102 PCR-recA-RFLP-HaeIII-AT–pattern clone. The emergence of certain bacterial phenotypes in the chronic infection such as the nonmucoid phenotype, small colony variants, brownish pigmented colonies, and hypermutators, proved to be, together with co-infection with Pseudomonas aeruginosa, the possible markers of more challenging infections and poor prognosis. The presence of co-colonizers and the bacterial phenotypes that are especially adapted to persist in long-term respiratory tract infections have a crucial role in patients' clinical outcomes.