The time to flowering is a key component of the life-history strategy of the model plant Arabidopsis thaliana that varies quantitatively among genotypes. A significant problem for evolutionary and ecological genetics is to understand how natural selection may operate on this ecologically significant trait. Here, we conduct a population genomic study of resequencing data from 52 genes in the flowering time network. McDonald-Kreitman tests of neutrality suggested a strong excess of amino acid polymorphism when pooling across loci. This excess of replacement polymorphism across the flowering time network and a skewed derived frequency spectrum toward rare alleles for both replacement and noncoding polymorphisms relative to synonymous changes is consistent with a large class of deleterious polymorphisms segregating in these genes. Assuming selective neutrality of synonymous changes, we estimate that approximately 30% of amino acid polymorphisms are deleterious. Evidence of adaptive substitution is less prominent in our analysis. The photoperiod regulatory gene, CO, and a gibberellic acid transcription factor, AtMYB33, show evidence of adaptive fixation of amino acid mutations. A test for extended haplotypes revealed no examples of flowering time alleles with haplotypes comparable in length to those associated with the null fri(Col) allele reported previously. This suggests that the FRI gene likely has a uniquely intense or recent history of selection among the flowering time genes considered here. Although there is some evidence for adaptive evolution in these life-history genes, it appears that slightly deleterious polymorphisms are a major component of natural molecular variation in the flowering time network of A. thaliana.