The focus of researchers, media and policy on doping in cycling is often limited to the professional level of the sport. However, anti-doping test results since 2001 demonstrate that banned substances are also used by US cyclists at lower levels of the sport, necessitating a broader view of the patterns and motivations of substance use within the sport. In this article, we describe and explain the doping culture that has emerged in domestic US cycling among amateur and semi-professionals. Through analysis of records from sports governing bodies and journalistic reports, we assess the range of violation types and discuss the detection and punishing of riders who were not proven to have intended to cheat but became “collateral damage” in the war on doping. We argue that the phenomenon of doping is more complex than what has been shown to occur in elite sport, as it includes a wider variety of behaviours, situations and motivations. We develop fresh insights by examining cases where doping has been accidental, intrinsically motivated, non-performance enhancing or the result of prescribed medical treatments banned by anti-doping authorities. Such trends call into question the fairness of anti-doping measures, and we discuss the possibility of developing localised solutions to testing and sanctioning amateur athletes.