Most organisms have evolved a timing mechanism or circadian clock that is able to generate 24 h rhythmic oscillations in multiple biological events. The environmental fluctuations in light and temperature synchronize the expression and activity of key oscillator components that ultimately define the period, phase and amplitude of output rhythms. In Arabidopsis, overexpression of the casein kinase 2 (CK2) regulatory subunits, CKB3 or CKB4, alters the function of the clock under free-running conditions, and results in period-shortening of genes peaking at different phase angles. Here, we examine the effects of CKB4 overexpression (CKB4-ox) on a number of clock outputs that are modulated by day length or photoperiod. We have found a phase shift in gene expression, shortening of hypocotyl elongation and earlier than wild-type initiation of flowering under short-day conditions. Our study shows that the earlier expression phases of the floral induction genes GIGANTEA, FLAVIN-BINDING KELCH REPEAT F-BOX1 and CONSTANS correlate with higher abundance of the FLOWERING LOCUS T transcript under short-day conditions. Matching the period of the external light/dark cycles relative to the endogenous short period of the CKB4-ox oscillator restores the phase of gene expression and the flowering sensitivity to day length, indicating that a clock defect is responsible for the CKB4-ox phenotypes. Our studies suggest a function for CKB4 very close to the oscillator, as expression of the core components TIMING OF CAB EXPRESSION 1 and CIRCADIAN CLOCK ASSOCIATED 1 is also altered in CKB4-ox plants. Based on our results, we propose that oscillator dysfunction is responsible for the period defect of CKB4-ox plants that leads to clock dissonance with the environment and reduced sensitivity to day length.