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Plants are associated with microbial communities, which are inherited through the seed and acquired from the environment. These microbiomes influence plant physiology, chemistry, and functioning. Yet, we lack insights into how seed origin and the environmental microbiome jointly influence the leaf metabolome. We used untargeted metabolomics (gas chromatography/mass spectrometry) on leaves of pedunculate oak (Quercus robur) seedlings to examine metabolic responses to different seed origins and environmental microbiomes, as well as home and away environments. For this, acorns were collected from three mother trees and grown in a multifactorial design with soil and canopy microbiomes originating from the local mother tree (i.e., the home treatment) and neighbouring trees (i.e., the away treatment). We also measured two plant traits—plant height and leaf chlorophyll content—to examine relationships between plant traits and the metabolome. The leaf metabolome did not differ significantly between plants growing with different soil and canopy microbiomes. However, the leaf metabolome differed among acorn origins and between seedlings growing in home vs. away treatments. We found no clear link between plant traits and the leaf metabolome. This study is one of the first to disentangle the combined effects of seed origin and environmental microbiomes on plant leaf chemistry, and the home vs. away framework provides novel insights into local adaptation effects on plant metabolomes within forest ecosystems. These findings have practical implications for the use of local genotypes and the development of microorganism-based management practices in sustainable forestry and agriculture.