Speaking involves coordination of multiple neuromotor systems, including respiration, phonation and articulation. Developing non-invasive imaging methods to study how the brain controls these systems is critical for understanding the neurobiology of speech production. Recent models and animal research suggest that regions beyond the primary motor cortex (M1) help orchestrate the neuromotor control needed for speaking, including cortical and sub-cortical regions. Using contrasts between speech conditions with controlled respiratory behavior, this fMRI study investigates articulatory gestures involving the tongue, lips and velum (i.e., alveolars versus bilabials, and nasals versus orals), and phonatory gestures (i.e., voiced versus whispered speech). Multivariate pattern analysis (MVPA) was used to decode articulatory gestures in M1, cerebellum and basal ganglia. Furthermore, apart from confirming the role of a mid-M1 region for phonation, we found that a dorsal M1 region, linked to respiratory control, showed significant differences for voiced compared to whispered speech despite matched lung volume observations. This region was also functionally connected to tongue and lip M1 seed regions, underlying its importance in the coordination of speech. Our study confirms and extends current knowledge regarding the neural mechanisms underlying neuromotor speech control, which hold promise to study neural dysfunctions involved in motor-speech disorders non-invasively.