Past work has demonstrated a link between semantic memory and verbal creativity. Yet, few studies have considered this relationship through the lens of the controlled semantic cognition account, which anticipates that multimodal concepts in long-term memory interact with semantic control processes to generate goal and context-appropriate patterns of retrieval. In particular, while the creativity literature has distinguished divergent and convergent aspects of creativity, little is known about their relationship with separable aspects of semantic control, or the semantic intrinsic functional architecture of the brain. We investigated whether tasks with greater reliance on controlled semantic retrieval (assessed through weak association) versus semantic selection (assessed through semantic feature matching) were differentially linked to divergent creativity (assessed with the unusual uses task; UUT) and convergent creativity (assessed with the remote associates task; RAT). Better performance on the RAT was linked to semantic selection, while stronger performance on UUT was linked to more efficient retrieval of weak associations. We also examined individual differences in the intrinsic functional architecture of the semantic system using resting-state fMRI. Greater coupling between the anterior temporal lobe (multimodal semantic store) and left inferior frontal gyrus (in the semantic control network) was linked to stronger convergent creativity. This pathway also correlated with semantic feature matching performance, but not the retrieval of weak associations. In contrast, better divergent creativity was linked to greater coupling between left inferior frontal gyrus and language-related auditory-motor regions, and decoupling from the default mode and frontoparietal networks. These connections correlated with the retrieval of weak associations. Interestingly, while decoupling of LIFG with default mode and frontoparietal networks correlated with the retrieval of weak associations, coupling of LIFG with these networks correlated with semantic feature matching. These behavioural and neurocognitive dissociations show that semantic control and creativity are highly related yet multifaceted constructs that depend on the underlying intrinsic architecture of key sites related to semantic cognition.