Circadian rhythms are believed to be of great importance to plant growth and performance under fluctuating climate conditions. However, it is unclear how plants with a functioning circadian clock will respond to irregular light environments that disturb circadian-regulated parameters related to growth. Chrysanthemum (Chrysanthemum morifolium ‘Coral Charm’) was exposed to supplemental light provided as irregular light breaks during the night, achieved by controlling the light based on forecasted solar irradiance and electricity prices. Growth, in terms of carbon gain, was linearly correlated to both daylength and daily light integral. This response was observed irrespective of the irregularity of the light breaks and despite circadian-regulated processes of carbohydrate metabolism, chlorophyll fluorescence, and leaf chlorophyll content being affected. Leaf expansion and stem elongation occurred at a faster rate in plants grown in short days with irregular light breaks during the night period compared with plants grown in a climate with a consecutive long light period, showing that low average light intensity promoted expansion of the photosynthetic area of the plants. These results are important to gain an understanding of the relationship between circadian-regulated processes and plant growth. These results will also contribute to increased energy savings in the use of supplemental light in greenhouse production.