For tree species with long and overlapping generations, many evolutionary factors affect individuals in their lifetime, which makes the study of their adaptation to current and future selection pressures a complex task. Despite recent advances in genomics, such task is also hampered by very large genome sizes in conifers such as Pinus pinaster, our case study, and fitness-related traits are costly to obtain. Previous genetic research in P. pinaster has shown a strong genetic structure across its range into distinct gene pools, which are likely due to multiple refugia that survived previous glaciation periods and experienced expansions and contractions. These size changes thus probably impacted both molecular diversity and local adaptation patterns. Larger scale molecular data showed that candidate-gene single nucleotide polymorphisms linked to harsher environmental conditions could be used as proxies for natural population survival. Besides, a comparative study of the distribution of fitness effects with a more widespread conifer indicates a high rate of new adaptive substitutions. However, neither of these studies specifically model the demographic history of the species. Here we aimed at comparing demographic scenarios in a natural population from the Northern margin of the distribution, by applying approximate Bayesian computation methods to 29 gene sequences and ten microsatellites. Scenarios of population size reduction much better fitted the data than alternative Standard Neutral or expansion models, whether using both types of markers separately or together. Posterior distributions indicated a current effective population size of a few thousands individuals, compared to a much larger ancestral effective size. This confirms a strong size reduction, which likely dates back earlier than the last glacial maximum. We further tested departures from this demographic model across candidate genes with additional summary statistics, and observed outliers under putative balancing selection. Results implications on the adaptive potential of the maritime pine Aquitaine population are discussed in the context of future climatic changes and for the conservation and management of the more extended species distribution.