BackgroundThe fig (Ficus caricaL.) tree has high economic value. However, its fruit have a short shelf life due to rapid softening. Polygalacturonases (PGs) are essential hydrolases, responsible for the pectin degradation that plays a key role in fruit softening. However, figPGgenes and their regulators have not yet been characterized.ResultsIn this study, 43FcPGs were identified in the fig genome. They were non-uniformly distributed on 13 chromosomes, and tandem repeatPGgene clusters were found on chromosomes 4 and 5. Ka/Ks calculation and collinear analysis indicated negative selection as the main driver ofFcPGfamily expansion. FourteenFcPGs were found expressed in fig fruit with FPKM values > 10, of which seven were positively correlated, and three, negatively correlated with fruit softening. ElevenFcPGs were upregulated and two downregulated in response to ethephon treatment.FcPG12, a member of the tandem repeat cluster on chromosome 4, was selected for further analyses due to its sharp increment in transcript abundance during fruit softening and its response to ethephon treatment. Transient overexpression ofFcPG12led to decreased fig fruit firmness and increased PG enzyme activity in the tissue. Two ethylene response factor (ERF)-binding GCC-box sites were found on theFcPG12promoter. Yeast one-hybrid and dual luciferase assays showed thatFcERF5binds directly to theFcPG12promoter and upregulates its expression. Transient overexpression ofFcERF5upregulatedFcPG12expression, thereby increasing PG activity and fruit softening.ConclusionsOur study identifiedFcPG12as a keyPGgene in fig fruit softening, and its direct positive regulation byFcERF5. The results provide new information on the molecular regulation of fig fruit softening.Supplementary InformationThe online version contains supplementary material available at 10.1186/s12870-023-04315-7.