Flowering of the reference legumeMedicago truncatulais promoted by winter cold (vernalization) followed by long‐day photoperiods (VLD) similar to winter annual Arabidopsis. However, Medicago lacksFLCandCO, key regulators of Arabidopsis VLD flowering.Most plants have twoINHIBITOR OF GROWTH(ING) genes (ING1andING2), encoding proteins with an ING domain with two anti‐parallel alpha‐helices and a plant homeodomain (PHD) finger, but their genetic role has not been previously described.In Medicago,Mting1gene‐edited mutants developed and flowered normally, but anMting2‐1 Tnt1insertion mutant and gene‐editedMting2mutants had developmental abnormalities including delayed flowering particularly in VLD, compact architecture, abnormal leaves with extra leaflets but no trichomes, and smaller seeds and barrels.Mting2mutants had reduced expression of activators of flowering, including theFT‐like geneMtFTa1, and increased expression of the candidate repressorMtTFL1c, consistent with the delayed flowering of the mutant.MtING2overexpression complementedMting2‐1, but did not accelerate flowering in wild type. The MtING2 PHD finger bound H3K4me2/3 peptides weaklyin vitro, but analysis of gene‐edited mutants indicated that it was dispensable to MtING2 function in wild‐type plants. RNA sequencing experiments indicated that >7000 genes are mis‐expressed in theMting2‐1mutant, consistent with its strong mutant phenotypes. Interestingly, ChIP‐seq analysis identified >5000 novel H3K4me3 locations in the genome ofMting2‐1mutants compared to wild type R108. Overall, our mutant study has uncovered an important physiological role of a plantING2gene in development, flowering, and gene expression, which likely involves an epigenetic mechanism.