The context of John 10:16 reveals that Jesus is the shepherd of the “little flock” (Luke 12:32). These faithful followers are his chosen “sheep” who will work with him throughout all eternity upon their resurrection. This sheep class, his church, is now being called to be sacrificed just as the Lamb of God was sacrificed, “laying down their lives for the brethren” (1 John 3:16). It is the same flock spoken of in the 27th verse: “My sheep hear my voice and I know them, and they follow me. And I give them eternal life, and they shall never perish; neither shall anyone snatch them out of my hand.”

But the 16th verse shows there are two classes of sheep, led by the voice of the shepherd.

The original audience of these word was the nation of Israel to whom these heavenly promises were first offered. Israel rejected their Lord and was cast off.  Still, “they are beloved for the sake of their forefathers,” Romans 11:28 (NKJV). In Christ’s kingdom, the nation, while not receiving the more special heavenly promises, will be blessed: “For the gifts and the calling of God are irrevocable.” Romans 11:29 (NKJV).

These other sheep will also include all of mankind. Remember the prophecy of Daniel 2:44, “in the days of these kings shall the God of heaven set up a kingdom, which shall never be destroyed.” Yes, in God’s kingdom all people will be resurrected (John 5:28,29) and taught righteousness (Isaiah 26:9). Then mankind “will go out in joy and be led forth in peace; the mountains and hills will burst into song,” (Isaiah 55:12.) All lies will be swept away (Isaiah 28:17) and “the knowledge of the Lord will cover the earth as the waters cover the sea,” (Isaiah 11:9). Those who learn to love and obey the Lord during the coming millennial kingdom will become sheep. Though not of the heavenly fold, they will be blessed with eternal life here on earth.

Bible Commentary from William Barclay on this verse: “In the King James Version there is a mistranslation. It has: “There shall be one fold and one shepherd.” That mistranslation goes back to Jerome and the Vulgate. And on that mistranslation the Roman Catholic Church has based the teaching that, since there is only one fold, there can only be one Church, the Roman Catholic Church, and that, outside it there is no salvation. But the real translation beyond all possible doubt as given in the Revised Standard Version, is: “There shall be one flock, one shepherd,” or, even better, “They shall become one flock and there shall be one shepherd.” The unity comes from the fact, not that all the sheep are forced into one fold, but they all hear, answer and obey one shepherd. It is not an ecclesiastical unity; it is a unity of loyalty to Jesus Christ. The fact that there is one flock does not mean that there can be only one Church, one method of worship, one form of ecclesiastical administration. But it does mean that all the different churches are united by a common loyalty to Jesus Christ.”