The H1N1pdm09 influenza virus, which emerged in 2009 following a unique reassortment of swine-origin gene segments, rapidly replaced the seasonal H1N1 strain and triggered the first influenza pandemic of the twenty-first century. In Brazil, the virus initially spread through intense community transmission before establishing a pattern of seasonal circulation. However, its long-term evolutionary dynamics in the country remain insufficiently characterized. To address this gap, we conducted a coordinated national genomic surveillance effort focused on the period from 2014 onward, when Brazil began systematic whole-genome sequencing of circulating H1N1pdm09 viruses. Through collaborative sequencing across all five Brazilian macroregions, we generated 597 complete genomes collected between 2014 and 2024. Using phylodynamic approaches, we reconstructed the spatiotemporal spread of H1N1pdm09, identified major circulating lineages, and integrated epidemiological data to assess patterns of persistence and regional transmission. Our findings reveal sustained circulation and multiple independent viral introductions over the past decade, with evidence of localized lineage maintenance, particularly in the Southeast and South regions. Phylogenetic analyses also indicate repeated seeding from international sources, underscoring the continued impact of global viral movement. In addition, genome-wide comparisons revealed reassortment events involving internal segments, which may have contributed to the persistence and adaptation of dominant lineages following the COVID-19 pandemic. This study presents the most comprehensive reconstruction of H1N1pdm09 evolutionary dynamics in Brazil to date, highlighting the critical role of integrated, nationwide genomic surveillance in enhancing public health preparedness in tropical and subtropical regions.