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Summary Isogenic individuals can display seemingly stochastic phenotypic differences, limiting the accuracy of genotype‐to‐phenotype predictions. The extent of this phenotypic variation depends in part on genetic background, raising questions about the genes involved in controlling stochastic phenotypic variation.Focusing on early seedling traits inArabidopsis thaliana, we found that hypomorphs of the cuticle‐related geneLIPID TRANSFER PROTEIN 2(LTP2) greatly increased variation in seedling phenotypes, including hypocotyl length, gravitropism and cuticle permeability. Manyltp2hypocotyls were significantly shorter than wild‐type hypocotyls while others resembled the wild‐type.Differences in epidermal properties and gene expression betweenltp2seedlings with long and short hypocotyls suggest a loss of cuticle integrity as the primary determinant of the observed phenotypic variation. We identified environmental conditions that reveal or mask the increased variation inltp2hypomorphs and found that increased expression of its closest paralogLTP1is necessary forltp2phenotypes.Our results illustrate how decreased expression of a single gene can generate starkly increased phenotypic variation in isogenic individuals in response to an environmental challenge.