Fragile X Syndrome (FXS) is the most common heritable form of intellectual disability, affecting 1:4-6000 children, and a prominent genetic cause of Autism. Symptoms include cognitive impairment, seizures, and deficits in sensory processing including tactile hypersensitivity. Dissecting sensory cortical pathophysiology in FXS offers insight into both sensory dysfunction and higher cognitive impairment. Studies in the Fmr1-KO mouse model of FXS display developmental and lasting abnormalities in cortical neuronal physiology. In particular, altered plasticity at thalamocortical (TC) synapses, the principal cortical input for ascending sensory information, was shown in somatosensory cortex during the first 10 postnatal days. During this early critical period in wild-type (WT) mice, the temporal resolution of TC inputs undergoes coordinated developmental refinement to selectively promote cortical responsiveness to high frequency TC synaptic activity essential for high fidelity tactile coding and activity-dependent refinement of intracortical circuitry. Hypothesizing that abnormal presentation of sensory inputs at the first stage of cortical processing could both affect juvenile sensory perception in FXS and impair the maturation of cortical circuits, we examined TC input responses in the juvenile Fmr1-KO somatosensory cortical Layer 4 (L4) circuit. Synaptic integration, L4 connectivity and evoked network activity were investigated using whole-cell and Multi-Electrode Array electrophysiology in a TC brain slice preparation. Relative to WTs, Fmr1-KO L4 excitatory neurons displayed elevated intrinsic excitability, increased feed-forward inhibitory drive and altered TC synaptic kinetics. Intracortical connectivity between excitatory/excitatory and excitatory/inhibitory neurons was broadly reduced in Fmr1-KOs. Computational simulations of TC input integration informed by in vitro data suggested dynamic re-tuning of TC processing in Fmr1-KOs by distributed circuit mechanisms but an uncompensated hypersensitivity to high frequency stimulation. As predicted, thalamorecipient excitatory neurons in Fmr1-KO slices showed altered temporal resolution of TC inputs following thalamic stimulation with behaviourally relevant patterns. Significantly exaggerated voltage summation could be achieved in L4 excitatory neurons following burst stimulation at 20-50Hz, with abnormal recruitment of reverberant L4 network activity possible following 5-20Hz stimulation. Quantifying L4 network activity in Fmr1-KO slices demonstrated pronounced reductions in population response sparsity, spike rate and trial-to-trial fidelity in Fmr1-KOs, with reduced spatial spread of network activity. Together, these data demonstrate cortical hypersensitivity to TC inputs and abnormal recruitment of network activity by critical period Fmr1-KO somatosensory cortical circuits. The hyperresponsiveness and reduced fidelity of intracortical circuitry following behaviourally salient stimuli demonstrated in the present study may underlie tactile hyperexcitability and abnormal sensory discrimination in FXS patients, and likely contribute to deleterious cortical development.