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According to a conventional evolutionary perspective, the human propensity for substance use is the product of a ‘mismatch’ between emotional mechanisms that evolved in a past without pure drugs or direct routes of drug administration, and the occurrence of these phenomena in the contemporary environment. The primary purpose of this review is to assert that, contrary to the conventional view, humans have shared a co-evolutionary relationship with psychotropic plant substances that is millions of years old. We argue that this ‘deep time’ relationship is self-evident both in the extant chemical–ecological adaptations that have evolved in mammals to metabolize psychotropic plant substances and in the structure of plant defensive chemicals that have evolved to mimic the structure, and interfere with the function, of mammalian neurotransmitters. Given this evidence, we question how emotional mechanisms easily triggered by plant toxins can have evolved. Our argument is also supported with archeological and historical evidence of substance use in antiquity suggesting that, for people in the past, psychotropic plant substances were as much a mundane everyday item as they are for many people today. Our second, and more speculative objective is to suggest provisional hypotheses of human substance-using phenomena that can incorporate the evolutionary implications of a deep time relationship between psychotropic substances and people. We discuss hypotheses of selective benefits of substance use, including the idea that neurotransmitter-analog plant chemicals were exploited as substitutes for costly, nutritionally constrained endogenous neurotransmitters. However, even if substance seeking was adaptive in the environment of our hominid ancestors, it may not still be so in the contemporary environment. Thus, the implications of our argument are not that the mismatch concept does not apply to human substance-using phenomena, but that it must be reconsidered and extended to incorporate the implications of a substance-rich, rather than substance-free, evolutionary past.