Background: Individuals with chronic lung disease like cystic fibrosis often suffer from persistent bacterial infections, and prolonged antibiotic treatment contributes to antimicrobial resistance (AMR). Bacteriophage (phage) therapy is currently being revisited to treat AMR due to its specificity and lack of documented adverse effects. This study aimed to investigate host-phage-bacteria dynamics in the airway cells. Methods: Primary airway epithelial cells (pAECs) were established and differentiated at air-liquid interface (ALI) prior to inoculating with P. aeruginosa (PAO1, MIC74 and MIC90) over 24 hours to form biofilms. Phages (Kara-mokiny 3 (KM3), Boorn-mokiny 1 (BM1), Minga-mokiny 4 (MM4), and E79) were tagged using SYBR Gold DNA stain, filtered, and added onto airway cultures. The pAECs exposed to tagged phages were sorted using a BD LSR fortessa, and tagged phages were detected using the B530 filter set. Apical and basolateral collected supernatants were measured for IL-8 production and inserts were fixed and stained for various cell structures (ciliated cells, tight junction) and cell function (secretory mucin). Bactericidal activity was measured by viable P. aeruginosa enumeration. Results: Administration of different phage morphotypes, KM3, BM1, MM4, and E79 alone, did not significantly induce IL-8 production by pAECs over 24 h. Exposure of phages KM3 and MM4 to biofilms formed on ALIs culture had significantly reduced bacterial loads at 24 hours post-exposure with KM3 (3.8 x 109 ± SD vs 7.3 x 104 ± SD) and MM4 (3.5 x 109 ± SD vs 1.6 x 108 ± SD), respectively. Furthermore, infected pAECs treated with these phages did not induce additional IL-8 production basolaterally when compared to bacterial infected only pAECs (KM3: 3.9 ± 0.4 x 105, MM4: 3.6 ± 0.5 x 105 vs control: 2.6 ± 1.0 x 105 ). Conclusion: We demonstrated interactions between phages and airway cells in the presence or absence of a bacterial host, suggesting key implications for phage administration, safety, and efficacy.