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Abstract The environment can alter the magnitude of phenotypic variation among individuals, potentially influencing evolutionary trajectories. However, environmental influences on variation are complex and remain understudied. Populations in heterogeneous environments might exhibit more variation, the amount of variation could differ between benign and stressful conditions, and/or variation might manifest in different ways among stages of the gene‐to‐protein expression cascade or among physiological functions. Here, we explore these three issues by quantifying patterns of inter‐individual variation in both transcript and protein expression levels among California mussels,Mytilus californianusConrad. Mussels were exposed to five ecologically relevant treatments that varied in the mean and interindividual heterogeneity of body temperature. To target a diverse set of physiological functions, we assessed variation within 19 expression subnetworks, including canonical stress‐response pathways and empirically derived coexpression clusters that represent a diffuse set of cellular processes. Variation in expression was particularly pronounced in the treatments with high mean and heterogeneous body temperatures. However, with few exceptions, environment‐dependent shifts of variation in the transcriptome were not reflected in the proteome. A metric of phenotypic integration provided evidence for a greater degree of constraint on relative expression levels (i.e., stronger correlation) within expression subnetworks in benign, homogeneous environments. Our results suggest that environments that are more stressful on average – and which also tend to be more heterogeneous – can relax these expression constraints and reduce phenotypic integration within biochemical subnetworks. Context‐dependent “unmasking” of functional variation may contribute to interindividual differences in physiological phenotype and performance in stressful environments.