Auditory processing is widely understood to occur differently in autism, though the exact brain activity underlying these differences is not well understood. The diversity of autism also means there may be multiple ways the network can change to produce a similar behavioural output. We used larval zebrafish to investigate auditory habituation in four genetic models of autism: fmr1, mecp2, scn1lab and cntnap2. Larval zebrafish are optically transparent, enabling whole-brain imaging of neural activity at single-cell resolution using genetically encoded calcium indicator GCaMP6s. In free-swimming behavioural tests, we found all four autism model lines had different habituation characteristics from their wild-type siblings. We then imaged brain activity using selective plane illumination microscopy. Using correlation to auditory stimulus timings and fish movements, we identified auditory and motor responses throughout the brain. While we did not see any gross differences in responses in primary auditory areas, differences were apparent in brain regions associated with sensory integration and sensorimotor gating. The scn1lab mutants had the strongest behavioural phenotype, and had uniquely drastic reductions in habenular activity. We found an overlapping phenotype of anticorrelation to motor activity in the granule cells of the cerebellum in scn1lab and mecp2 fish, indicating some shared network dynamics underlying their behavioural phenotypes. We also found a bilateral nucleus in the hindbrain which responded very strongly in the beginning of the habituation period in fmr1 and cntnap2 mutants. These results indicate distinct but overlapping circuit changes underlying the different habituation phenotypes in the four different genetic lines.