Donor and recipient HCMV-seropositive (D+R+) lung transplant recipients (LTRs) often harbour multiple human cytomegalovirus (HCMV) strains, likely due to transmitted donor (D) strains and reactivated recipient (R) strains. To date, the extent and timely occurrence of each likely source in shaping the post-transplantation (post-Tx) strain population is unknown. Here, we deciphered the D and R origin of the post-Tx HCMV strain composition in blood, bronchoalveolar lavage (BAL), and CD45+ BAL cell subsets. We investigated either D and/or R formalin-fixed paraffin-embedded blocks or fresh D lung tissue from four D+R+ LTRs obtained prior to transplantation. HCMV strains were characterised by short amplicon deep sequencing. In two LTRs, we show that the transplanted lung is reseeded by R strains within the first six months after transplantation, likely by infiltrating CD14+ CD163+/- alveolar macrophages. In three LTRs, we demonstrate both rapid D-strain dissemination and persistence in the transplanted lung for >1 year post-Tx. Broad inter-host diversity contrasts with intra-host genotype sequence stability upon transmission, during follow-up and across compartments. In D+R+ LTRs, HCMV strains of both, D and R origin can emerge first and dominate long‑term in subsequent episodes of infection, suggesting no replication advantage of one source over the other despite pre-existing R strain-specific immunity.