The genioglossus (GG) muscle is divided into horizontal and oblique compartments that are the main protrusor and depressor muscles of the tongue, respectively. In humans the GG plays an important role in speech articulation, swallowing, and inspiratory dilation of the pharynx. At present, little is known about the neuromuscular specializations of the GG in any mammal. This study examined the specializations of these compartments in the canine tongue using a variety of anatomical and histochemical techniques. Six canine GG muscles were sectioned and stained for myofibrillar ATPase to study muscle fiber types; five whole-mount GG muscles were stained for acetylcholinesterase (AChE) to study the distribution of motor endplates; and eight whole mount GG muscles were processed with Sihler's stain to study the entire nerve supply pattern. In addition, the arrangement of muscle fibers of the GG within the tongue was also determined (N = 3). The most notable difference between the compartments of the GG was their proportions of fast and slow twitch muscle fibers: the horizontal compartment contained 64% slow twitch muscle fibers compared to 41% in the oblique compartment. In addition, although the oblique compartment appeared to be grossly homogeneous, it could be divided into thirds by significant differences in the percentages of slow twitch fibers: posterior (23%), middle (15%), and anterior (56%; P < 0.05). The muscle fibers of the oblique GG within the tongue were found to be divided into medial and lateral layers that run vertically and transversely, respectively. The nerve supply to each third of the oblique GG formed a plexus with the anterior third being the densest. The innervation pattern of the oblique GG was also notable as terminal nerve branches coursing parallel to the muscle fascicles gave off perpendicular secondary branches along each motor endplate band. These secondary nerve branches connected the primary nerves and formed a regularly spaced grid throughout the compartment. Evidently, the two compartments of the GG exhibited different anatomical specializations. The horizontal had a slow muscle fiber profile and simple innervation pattern; these qualities are possibly related to its single force vector and respiratory related activity. The oblique compartment had a relatively fast muscle fiber profile with evidence for three separate functional subdivisions. The most anterior part was noticeably different, and was presumably specialized for fine motor control of the tip of the tongue. The vertically oriented fibers of the oblique GG within the tongue body may function as a midline depressor of the tongue, whereas its transversely oriented fibers could play a role in narrowing the tongue during other motor tasks.