The precise regulation of flowering timing is essential for plants’ success in reproduction and survival in natural environments. Seasonal changes in spring induce flowering by expressing florigen, FLOWERING LOCUS T (FT), in Arabidopsis. FT is expressed in unique phloem companion cells with unknown characteristics. It remained elusive which genes are co-expressed with FT and whether they also have roles in flowering. Through tissue-specific (TRAP-seq) translatome analysis in the FT-producing cells, we discovered that under long-day conditions with the natural sunlight red/far-red ratio, the FT-producing cells express the gene encoding small FPF1-LIKE PROTEIN 1 (FLP1) protein. The master FT regulator, CONSTANS (CO), controls FLP1 expression, suggesting FLP1’s involvement in the photoperiod pathway. FLP1 promotes early flowering independently of FT, is active in the shoot apical meristem, and induces the expression of SEPALLATA 3 (SEP3), a key E-class homeotic gene. Unlike FT, FLP1 facilitates inflorescence stem elongation. Our cumulative evidence indicates that FLP1 may act as a mobile signal. Thus, FLP1 orchestrates floral initiation together with FT and promotes inflorescence stem elongation during reproductive transitions.