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Sirtuins (SRTs) are a group of nicotinamide adenine dinucleotide (NAD+)‐dependent deacetylase that target both histone and nonhistone proteins. The biological function of SRT in horticultural plants has been rarely studied. In this study, FaSRT1‐2 was identified as a key member of the 8 FaSRTs encoded in cultivated strawberry genome. Transient overexpression of FaSRT1‐2 in strawberry fruit accelerated ripening, increased the content of anthocyanins and sugars, enhanced ripening‐related gene expression. Moreover, stable transformation of FaSRT1‐2 in strawberry plants resulted in enhanced vegetative growth, increased sensitivity to heat stress and increased susceptibility to Botrytis cinerea infection. Interestingly, knocking out the homologous gene in woodland strawberry had the opposite effects. Additionally, we found the content of stress‐related hormone abscisic acid (ABA) was decreased, while the growth‐related gibberellin (GA) concentration was increased in FaSRT1‐2 overexpression lines. Gene expression analysis revealed induction of heat shock proteins, transcription factors, stress‐related and antioxidant genes in the FaSRT1‐2‐overexpressed plants while knocked‐out of the gene had the opposite impact. In conclusion, our findings demonstrated that FaSRT1‐2 could positively promote strawberry plant vegetative growth and fruit ripening by affecting ABA and GA pathways. However, it negatively regulates the resistance to heat stress and B. cinerea infection by influencing the related gene expression. Summary statement: FaSRT1‐2 is likely to exert a positive regulatory effect on both strawberry fruit ripening and vegetative growth by stimulating sugar, anthocyanin, and the gibberellin metabolism pathway. Moreover, FaSRT1‐2 appears to enhance the susceptibility of strawberry plants to heat stress while also promoting defence against Botrytis cinerea through alterations in abscisic acid metabolism and stress‐related genes expression. [ABSTRACT FROM AUTHOR]