Growth is an integrative trait that responds to environmental factors and is crucial for plant fitness. A major environmental factor influencing plant growth is nutrient supply. In order to explore this relationship further, we quantified growth-related traits, ion content, and other biochemical traits (protein, hexose, and chlorophyll contents) of a recombinant inbred line population of Arabidopsis (Arabidopsis thaliana) grown on different levels of potassium and phosphate. Performing an all subsets multiple regression analyses revealed a link between growth-related traits and mineral nutrient content. Based on our results, up to 85% of growth variation can be explained by variation in ion content, highlighting the importance of ionomics for a broader understanding of plant growth. In addition, quantitative trait loci (QTLs) were detected for growth-related traits, ion content, further biochemical traits, and their responses to reduced supplies of potassium or phosphate. Colocalization of these QTLs is explored, and candidate genes are discussed. A QTL for rosette weight response to reduced potassium supply was identified on the bottom of chromosome 5, and its effects were validated using selected near isogenic lines. These lines retained over 20% more rosette weight in reduced potassium supply, accompanied by an increase in potassium content in their leaves.