Many plants undergo adaptation to fire. Yet, as global change is increasing fire frequency worldwide, our understanding of the genetics of adaptation to fire is still limited. We studied the genetic basis of serotiny (the ability to disseminate seeds exclusively after fire) in the widespread, pioneer Mediterranean conifer Pinus halepensis Mill., by linking individual variation in serotiny presence and level to fire frequency and to genetic polymorphism in natural populations. After filtering steps, 885 single nucleotide polymorphisms (SNPs) out of 8000 SNPs used for genotyping were implemented to perform an in situ association study between genotypes and serotiny presence and level. To identify serotiny-associated loci, we performed random forest analyses of the effect of SNPs on serotiny levels, while controlling for tree size, frequency of wildfires, and background environmental parameters. Serotiny showed a bimodal distribution, with serotinous trees more frequent in populations exposed to fire in their recent history. Twenty-two SNPs found in genes involved in stress tolerance were associated with the presence-absence of serotiny while 37 found in genes controlling for flowering were associated with continuous serotiny variation. This study shows the high potential of P. halepensis to adapt to changing fire regimes, benefiting from a large and flexible genetic basis of trait variation.