Peanut (Arachis hypogaea) is a crop plant with high economic value, but the epigenetic regulation of its growth and development has only rarely been studied. The peanut histone deacetylase 1 gene (AhHDA1) has been isolated and is known to be ABA- and drought-responsive. In this paper, we investigate the role of AhHDA1 in more detail, focussing on the effect of altered AhHDA1 expression in hairy roots at both the phenotypic and transcriptional levels. Agrobacterium rhizogenes-mediated transformation of A. hypogaea hairy roots was used to analyse how overexpression or RNA interference of AhHDA1 affects this tissue. In both types of transgenic hairy root, RNA sequencing was adopted to identify genes that were differentially expressed, and these genes were assigned to specific metabolic pathways. AhHDA1-overexpressing hairy roots were growth-retarded after 20 d in vitro cultivation, and superoxide anions and hydrogen peroxide accumulated to a greater extent than in control or RNAi groups. Overexpression of AhHDA1 is likely to accelerate flux through various secondary synthetic metabolic pathways in hairy roots, as well as reduce photosynthesis and oxidative phosphorylation. Genes encoding the critical enzymes caffeoyl-CoA O-methyltransferase (Araip.XGB85) and caffeic acid 3-O-methyltransferase (Araip.Z3XZX) in the phenylpropanoid biosynthesis pathway, chalcone synthase (Araip.B8TJ0) and polyketide reductase (Araip.MKZ27) in the flavonoid biosynthesis pathway, and hydroxyisoflavanone synthase (Araip.0P3RJ) and isoflavone 2'-hydroxylase (Araip.S5EJ7) in the isoflavonoid biosynthesis pathway were significantly upregulated by AhHDA1 overexpression, while their expression in AhHDA1-RNAi and control hairy roots remained at a lower level or was unchanged. Our results suggest that alteration of secondary metabolism activities is related to overexpression of AhHDA1, which is mainly reflected in phenylpropanoid, flavonoid and flavonoid biosynthesis. Future studies will focus on the function of AhHDA1 interacting proteins and their action on cell growth and stress responses.