Copper (Cu) is an essential micronutrient required for growth and development of all living organisms. In plants, Cu deficiency delays flowering time, reduces fertility, and may cause sterility. How Cu regulates flowering time and fertility is not well-known. Here we show that the reduced fertility of copper-deficient plants stemmed from multiple factors including the abnormal stigma papillae development, the abolished gynoecium fertility, and the failure of anthers to dehisce. The latter defect was associated with reduced lignification, the upregulation of copper microRNAs and the downregulation of their targets, laccases, implicated in lignin synthesis. Cu deficiency also decreased pollen viability and germination. These defects were associated with the reduced activity of the cytochrome c oxidase in leaves and the accumulation of reactive oxygen species in pollen grains, suggesting that altered energy level and redox status are contributing factors to reduced pollen germination. Using confocal x-ray fluorescence microscopy, we mapped Cu accumulation in pollen grains. This result corroborates with the fact that application of Cu directly to pollen germination media rescues the pollen germination defect of Cu-deficient plants. Further, we show that among copper deficiency-caused defects in Arabidopsis thaliana were also the increased shoot branching and delayed flowering. The increased shoot branching of copper-deficient plants was rescued by the exogenous application of auxin or Cu. The late-flowering phenotype of Cu-deficient plants is associated with the decreased transcript abundance of the Flowering Locus T (FT). Together, these results provide novel insights into the multifaceted functions of Cu in plant development and fertility.