HEXOKINASE 1 (HXK1) is an evolutionarily conserved glycolytic enzyme that has a separate nuclear glucose-sensor signalling function. In Arabidopsis, HXK1 mutant seedlings have a stunted growth defect, yet how this relates to HXK1 function remains inconclusive. We show that the HXK1-glycolytic pathway performs a fundamental role in catabolising seed reserves to fuel post-germinative cell division and expansion. This function is particularly important in dim light which delays the switch to photoautotrophic growth. RNAseq analysis reveals that HXK1 imposes strong repressive control on plastome gene expression, and regulates nuclear-encoded genes that drive energy-consuming processes. Earlier studies have implicated HXK1 sensor-signalling in the repression of CAB2 and CAA gene expression by exogenous glucose. We show that over a wide range of irradiances this pathway is not operative in seedlings. Our study therefore defines a new operational model for HXK1 action in catabolising carbon resources and tuning gene expression to optimize seedling growth.