Regulation of flowering by endogenous and environmental signals ensures that reproduction occurs under optimal conditions to maximize reproductive success. Involvement of the growth regulator gibberellin (GA) in the control of flowering by environmental cues varies among species. Arabis alpina Pajares, a model perennial member of the Brassicaceae, only undergoes floral induction during vernalization, allowing definition of the role of GA specifically in this process. The transcription factor PERPETUAL FLOWERING1 (PEP1) represses flowering until its mRNA levels are reduced during vernalization. Genome-wide analyses of PEP1 targets identified genes involved in GA metabolism and signaling, and many of the binding sites in these genes were specific to the A. alpina lineage. Here, we show that the pep1 mutant exhibits an elongated-stem phenotype, similar to that caused by treatment with exogenous GA, consistent with PEP1 repressing GA responses. Moreover, in comparison with the wild type, the pep1 mutant contains higher GA4 levels and is more sensitive to GA prior to vernalization. Upon exposure to cold temperatures, GA levels fall to low levels in the pep1 mutant and in wild-type plants, but GA still promotes floral induction and the transcription of floral meristem identity genes during vernalization. Reducing GA levels strongly impairs flowering and inflorescence development in response to short vernalization treatments, but longer treatments overcome the requirement for GA. Thus, GA accelerates the floral transition during vernalization in A. alpina, the down-regulation of PEP1 likely increases GA sensitivity, and GA responses contribute to determining the length of vernalization required for flowering and reproduction.