The human jaw-closing and jaw-opening muscles produce forces leading to the development of three-dimensional bite and chewing forces and to three-dimensional movements of the jaw. The length of the sarcomeres is a major determinant for both force and velocity, and the maximal work, force, and shortening range each muscle is capable of producing are proportional to the architectural parameter volume, physiological cross-sectional area, and fiber length, respectively. In addition, the mechanical role the muscles play is strongly related to their three-dimensional position and orientation in the muscle-bone-joint system. The objective of this study was to compare relevant architectural characteristics for the jaw-closing and jaw-opening muscles and to provide a set of data that can be used in biomechanical modeling of the masticatory system. In eight cadavers, sarcomere lengths, muscle masses, fiber lengths, pennation angles, and physiological cross-sectional areas were determined for the following muscles: superficial and deep masseter, anterior and posterior temporalis, anterior and posterior medial pterygoid, inferior and superior lateral pterygoid, posterior and anterior digastric, geniohyoid, posterior and anterior mylohyoid, and stylohyoid. To determine the spatial position of their action lines, the three-dimensional coordinates of the attachment sites were registered. Compared with the jaw openers, the jaw closers were characterized by shorter sarcomere lengths at the closed jaw, larger masses of contractile and tendinous tissue, larger physiological cross-sectional areas, larger pennation angles, shorter fiber lengths, shorter moment arms, and lower fiber-length-to-muscle-length ratios. In addition, architectural features differed across the muscles of the same functional group. Sarcomere length did not differ significantly among the regions of the same muscle. In contrast, in some muscles, significant intramuscular differences were found with respect to, e.g., physiological cross-sectional area, fiber length, pennation angle, and moment arm length. The results suggest that the jaw-closing muscles have architectural features that suit them for force production. Conversely, the jaw-opening muscles are better designed to produce velocity and displacement.