Psychiatric conditions are frequently accompanied by altered blood metabolite profiles, yet it remains unclear whether these reflect shared biology, causal pathways, or secondary consequences of illness. Emerging evidence suggests there is a genetic relationship between metabolites and psychiatric traits requiring further investigation to uncover clinically actionable biology. To address this, we leveraged the largest genome-wide association studies (GWAS) available to systematically map genetic correlations and causal relationships between 249 circulating metabolites and 10 major psychiatric conditions. After multiple testing correction, we identified 1,100 significant genetic correlations, revealing condition-specific patterns of metabolic architecture dominated by lipoprotein and fatty acid traits. Latent causal variable modelling and a Bayesian Mendelian randomisation framework (CAUSE) further identified metabolites with evidence for causal effects. Notably, high-density lipoprotein particle traits were associated with increased liability for anorexia nervosa, while low- and very-low-density lipoprotein traits were linked to risk for attention deficit/hyperactivity disorder (ADHD), major depressive disorder, obsessive compulsive disorder, and post-traumatic stress disorder. Interestingly, docosahexaenoic acid and omega-3 fatty acids exhibited evidence for protective effects in ADHD, consistent with previous randomised controlled trials. Several metabolites showing evidence for causal relationships with psychiatric traits were also causally associated with cortical structure, although mediation uncovered limited evidence for mediation. Using CAUSE, we further identified 23 metabolite-psychiatric trait pairings with stronger evidence for shared genetic architecture than direct causality. Gene prioritisation for these pairs revealed convergence on neuronal, metabolic and signalling pathways including MAPK, BDNF and serotonin receptor signalling, among others. These findings highlight mechanistic overlap between metabolic and psychiatric traits and identify clinically actionable metabolites with potential for therapeutic targeting or biomarker development. Together, this work establishes a comprehensive genetic atlas of circulating metabolite-psychiatric trait relationships, providing a valuable resource for disentangling metabolic contributions to psychiatric risk and guiding precision intervention strategies.