The genetic basis of growth and development is often studied in constant laboratory environments; however, the environmental conditions that organisms experience in nature are often much more dynamic. We examined how daily temperature fluctuations, average temperature, day length and vernalization influence the flowering time of 59 genotypes of Arabidopsis thaliana with allelic perturbations known to affect flowering time. For a subset of genotypes, we also assessed treatment effects on morphology and growth. We identified 17 genotypes, many of which have high levels of the floral repressor FLOWERING LOCUS C (FLC), that bolted dramatically earlier in fluctuating - as opposed to constant - warm temperatures (mean = 22°C). This acceleration was not caused by transient VERNALIZATION INSENSITIVE 3-mediated vernalization, differential growth rates or exposure to high temperatures, and was not apparent when the average temperature was cool (mean = 12°C). Further, in constant temperatures, contrary to physiological expectations, these genotypes flowered more rapidly in cool than in warm environments. Fluctuating temperatures often reversed these responses, restoring faster bolting in warm conditions. Independently of bolting time, warm fluctuating temperature profiles also caused morphological changes associated with shade avoidance or 'high-temperature' phenotypes. Our results suggest that previous studies have overestimated the effect of the floral repressor FLC on flowering time by using constant temperature laboratory conditions.