Jesus had just told them to labour for food that lasts. They took up His word and asked what labour God wanted from them. Barnes takes them as sincere: they meant works "God will approve," and he calls it "the earnest inquiry of men who were seeking to be saved," though he adds that they expected to find the way of life "by their works." Gill reads it less kindly. He sees in it the usual habit of the people, seeking righteousness and life not by faith but by the works of the law. Either way, they were thinking in terms of works they could do.

Jesus answered at once: "This is the work of God, that ye believe on him whom he hath sent" (John 6:29). They asked about "works"; He named one "work." Barnes explains it as the thing "which you are to do in order to be saved." The crowd then asked Him for a sign (John 6:30), and the conversation led to His words, "I am the bread of life" (John 6:35).

The KJV phrase "work the works" echoes the Greek, which uses a verb and a noun from the same root: ergazōmetha ta erga, "that we might be working the works." Jesus had used the same verb (ergazesthe) a moment earlier: "Labour not for the meat which perisheth" (John 6:27). His answer turns their plural "works" (erga) into a single "work" (ergon): to believe (John 6:29).

This crowd had followed Jesus because they "did eat of the loaves, and were filled" (John 6:26). The day before, after the miracle, some had said, "This is of a truth that prophet that should come into the world," and Jesus withdrew when they wanted to make Him king by force (John 6:14-15).

This question shows how God's way differs from ours. People naturally ask, "What must we do?" Jesus' answer is that the one work God asks is to believe on the One He sent. Later in the same teaching He says, "this is the will of him that sent me, that every one which seeth the Son, and believeth on him, may have everlasting life" (John 6:40).

Believing is not doing nothing. Matthew Henry calls the "Constant exercise of faith in Christ" the "most important and difficult part of the obedience required from us." Barnes notes that Jesus "did not tell them they had nothing to do, or that they were to sit down and wait"; the work was to believe on the Messiah.