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Loblolly pine (Pinus taeda) and slash pine (Pinus elliottii) are ecologically and economically important pine species that dominate many forest ecosystems in the southern United States, but like all conifers, the study of their genetic diversity and demographic history has been hampered by their large genome size. A small number of studies mainly based on candidate-gene sequencing have been reported for P. taeda to date, whereas none are available for P. elliottii. Targeted exome resequencing has recently enabled population genomics studies for conifers, approach used here to assess genomic diversity, signatures of selection, population structure, and demographic history of P. elliottii and P. taeda. Extensive similarities were revealed between these species: both species feature rapid linkage disequilibrium decay and high levels of genetic diversity. Moreover, genome-wide positive correlations for measures of genetic diversity between the species were also observed, likely due to shared structural genomic constraints. Also, positive selection appears to be targeting a common set of genes in both pines. Demographic history differs between both species, with only P. taeda being affected by a dramatic bottleneck during the last glacial period. The ability of P. taeda to recover from a dramatic reduction in population size while still retaining high levels of genetic diversity shows promise for other pines facing environmental stressors associated with climate change, indicating that these too may be able to adapt successfully to new future conditions even after a drastic population size contraction.