Polycomb Group (PcG) proteins play important roles in regulating developmental phase transitions in plants; however, little is known about the role the PcG machinery in regulating the transition from juvenile to adult phase. Here, we show that Arabidopsis BMI1 (AtBMI1) PRC1 components participate in the repression of miR156. Loss of AtBMI1 function leads to upregulation of pri-MIR156A/C at the time the levels of miR156 should decline, resulting in an extended juvenile phase and delayed flowering. Conversely, the PRC1 component EMBRYONIC FLOWER (EMF1) participates in the regulation of SPL and MIR172 genes. Accordingly, plants impaired in EMF1 function displayed misexpression of these genes early in development, which contributes to a CONSTANS (CO)-independent upregulation of FLOWERING LOCUS T (FT) leading to the earliest flowering phenotype described in Arabidopsis. Our findings show how the different regulatory roles of two functional PRC1 variants coordinate the acquisition of flowering competence and help to reach the threshold of FT necessary to flower. Furthermore, we show how two central regulatory mechanisms, such as PcG and miRNA, assemble to achieve a developmental outcome.