Determining the genetic basis of speech and language disorders provides insight into the neurobiology of human communication. Despite intensive investigation, the molecular aetiology of speech disorder remains unexplained in most children. We investigated a cohort of 34 children with suspected severe childhood speech disorder. After detailed phenotypic profiling, 32 had a confirmed diagnosis of childhood apraxia of speech (CAS) and two had severe phonological disorder, as well as a range of co-occurring neurodevelopmental features. We sequenced whole genomes or exomes of these 34 children on a research basis, and clinical microarray analysis was conducted for 15. In 11/34 (32%) of probands, we identified a pathogenic single nucleotide (n = 10) or copy number (n = 1) variant in novel genes or loci for CAS that have been implicated in neurodevelopmental disorders: CDK13, EBF3, GNAO1, GNB1, DDX3X, MEIS2, POGZ, SETBP1, UPF2, ZNF142, and the 5q14.3q21.1 locus. In nine of these probands the variants were confirmed de novo by screening parental DNA. Seven of these genes encode proteins critical for regulation of gene transcription. In parallel collaborative work found pathogenic variants in additional families with severe childhood speech disorder in DDX3X, SETBP1, UPF2, and ZNF142. In one proband, we identified a large mosaic deletion at 5q14.3q21.1 that included two genes (CHD1, NR2F1) linked to neurodevelopmental disorders. We performed gene co-expression analyses on these genes and identified at least one distinct network of regulatory genes emerging from our molecular screening of CAS. Our findings underscore the importance of transcriptional regulation during speech development.