Both membrane progestin receptors (mPRs) and the nuclear progestin receptor (nPR or Pgr) decode the non-genomic progestin signaling (NGPS) in vertebrates. However, the receptor for deciphering extracellular NGPS and initiating meiosis resumption in vertebrate oocytes is still contested hotly. We studied the roles of nPR and mPRs by determining their localization, changes of expression, and activation of NGPS during final oocyte maturation (FOM) in zebrafish. The nPR transcript and protein were expressed abundantly in follicular cells that were surrounding stage IV oocytes, but nPR transcript appeared absent within stage IV oocytes. The most significant daily changes of nPR transcript were observed in stage IV follicular cells, with the highest level observed just prior to ovulation. In contrast, the expressions of mPRα and mPRβ transcripts and proteins were abundant and increased significantly in late stage denuded oocytes prior to oocyte maturation, consistent with the purported role of mPRs in interpreting NGPS. Moreover, over-expression of mPRα in follicle-enclosed oocytes significantly increased the activity of MAPK, the production of cyclin B protein, and the number of oocytes that underwent FOM without exogenous progestin, while over-expression of mPRβ or nPR alone had no such effect. Intriguingly, significant acceleration of FOM was observed when follicle-enclosed oocytes were incubated with the maturation inducing steroid, 4-pregnen-17, 20β-diol-3-one (DHP) following over-expression of nPR or mPRα. Interestingly, this acceleration in oocyte maturation was observed approximately 1h later in oocytes over-expressing nPR compared to those over-expressing mPRα. Importantly, the acceleration of maturation in the nPR injected group was blocked by treatment with the transcription inhibitor actinomycin D, implying a requirement of the genomic signaling pathway, while the same treatment did not affect the accelerated rate of maturation in mPRα injected oocytes. Taken together, these results imply that nPR and mPRβ are unlikely receptors for inducing FOM, while mPRα is the long-sought-after nongenomic progestin receptor that deciphers extracellular NGPS to initiate meiosis resumption in follicle-enclosed zebrafish oocytes.