Abstract Background and purpose Psychophysiological factors may contribute to the development of temporomandibular disorders (TMD). Both local orofacial and systemic responses have been investigated. However, most studies have concentrated on physiological responding during cognitive challenges, while responses during painful tasks may be highly relevant for the development of chronic pain conditions. Moreover, the relationship between experimental challenges and physiological responding may be influenced by affective responses during the experimental tasks, an issue not often considered in the literature. Methods This study compared electromyography (EMG) of the left masseter and left trapezius muscles, orofacial and digital skin blood-flow (SBF), mean arterial pressure (MAP), and heart rate (HR) at rest, during orofacial isometric contraction, electrocutaneous pain stimulation of the left hand, pressure pain stimulation of the masseter muscle and the sternum, and three cognitive tasks (reading aloud, a simulated job interview, and visuomotoric tracking). The participants were 25 TMD patients and 25 matched pain-free controls, all females. Affective responses were assessed with the State part of the State-Trait Personality Inventory and with Visual Analogue Scales. Results Masseter EMG levels were significantly lower in the TMD group relative to the control group during jaw contraction, pressure pain stimulation, the relaxation periods, and cognitive tasks. SBF, MAP, and HR responses were largely similar in the two groups, with SBF responses to pain stimulation evident at lower levels of stimulation than previously found. The TMD patients reported significantly higher levels of negative affect during the experiment. Conclusions and implications The low EMG responses in the TMD group may be taken in support of the Pain Adaptation Model of musculoskeletal pain, in which reduced muscular activity serves to protect a painful area. However, it may also be supportive of the Integrated Pain Adaptation Model, where higher central nervous structures influence local muscular output. The group similarities in systemic physiological responding in combination with the elevated levels of negative state affect in the TMD patients confirm previous reports of psychosocial differences being more reliable indicators of TMD than generalized physiological responding.