Two primary areas of damage have been implicated in apraxia of speech (AOS) based on the time post-stroke: (1) the left inferior frontal gyrus (IFG) in acute patients, and (2) the left anterior insula (aIns) in chronic patients. While AOS is widely characterized as a disorder in motor speech planning, little is known about the specific contributions of each of these regions in speech. The purpose of this study was to investigate cortical activation during speech production with a specific focus on the aIns and the IFG in normal adults. While undergoing sparse fMRI, 30 normal adults completed a 30-minute speech-repetition task consisting of three-syllable nonwords that contained either (a) English (native) syllables or (b) non-English (novel) syllables. When the novel syllable productions were compared to the native syllable productions, greater neural activation was observed in the aIns and IFG, particularly during the first 10 min of the task when novelty was the greatest. Although activation in the aIns remained high throughout the task for novel productions, greater activation was clearly demonstrated when the initial 10 min was compared to the final 10 min of the task. These results suggest increased activity within an extensive neural network, including the aIns and IFG, when the motor speech system is taxed, such as during the production of novel speech. We speculate that the amount of left aIns recruitment during speech production may be related to the internal construction of the motor speech unit such that the degree of novelty/automaticity would result in more or less demands respectively. The role of the IFG as a storehouse and integrative processor for previously acquired routines is also discussed.