Weediness in ephemeral plants is commonly characterized by rapid cycling, prolific "all in" flowering, and loss of perenniality. Many species made transitions to weediness of this sort, which can be advantageous in high-disturbance or human associated habitats. The molecular basis of this shift, however, remains mostly mysterious. Here we use transcriptome sequencing, genome resequencing scans for selection, and stress tolerance assays to study a weedy population of the otherwise non-weedy Arabidopsis arenosa, an obligately outbreeding relative of A. thaliana. Though weedy A. arenosa is widespread, a single genetic lineage colonized railways throughout central and northern Europe. We show that railway plants, in contrast to plants from sheltered outcrops in hill/mountain regions, are rapid cycling, have lost vernalization requirement, show prolific flowering, and do not return to vegetative growth. Comparing transcriptomes of railway and mountain plants across timecourses with and without vernalization, we found railway plants have sharply abrogated vernalization responsiveness, and high constitutive expression of heat and cold-responsive genes. Railway plants also have strong constitutive heat shock and freezing tolerance compared with mountain plants, where tolerance must be induced. We found 20 genes with good evidence of selection in the railway population. One of these, LATE ELONGATED HYPOCOTYL (LHY) is known in A. thaliana to regulate many stress response genes we found to be differentially regulated among the distinct habitats. Our data suggest that beyond life history regulation, other traits like basal stress tolerance are also associated with the evolution of weediness in A. arenosa.