Frequently in the discussion about gifts of the Holy Spirit, the Bible’s command to pray in the Spirit3 will be brought up. The assumption here is that the few times the Bible actually talks about the Christian’s need to “pray in the Spirit” is synonymous to and evidence of a gift of the Holy Spirit. Some have tried to define this by looking to other preachers or theologians, but let’s simply take a look at any/only/all Scripture for an answer…

How Scripture answers "What does it mean to pray in the Spirit?"

To pray in the Spirit is first something that can only be done by believers4,6, or those that have been given the Holy Spirit5. Naturally, these should be individuals offering prayers that are “according to His will”7. Similarly, Paul contextualizes it as pertaining to those “in Christ Jesus” in a chapter dedicated to how a Christian should be living according to the Spirit and not according to the flesh1. There he explicitly defines what it means to pray in the Spirit:

  • WHO: the Holy Spirit, as directed by God,
  • WHAT: interceding for us with “inexpressible groanings”,
  • WHY: in order to compensate for our own human (or “fleshly” per the context) weakness.

Notably, the “HOW” is not answered in Scripture, and therefore not something we can answer. We are only told matter-of-factly that He “DOES”. The fact that those “in the Spirit” should “pray in the Spirit” is repeated a couple of other times3,4 in a way consistent with Paul’s definition (without offering further explanation on “HOW”) and in a way that comforts a Christian that may feel inadequate in their daily struggle. Also worth noting is a passage2 that some attempt to pull into this discussion, but with misapplication. Based on the context, Paul is clearly speaking about his own “spirit” (the essence of his spirituality as a human) versus God’s Holy Spirit that indwells him as a believer5 or the special, miraculous gifts he possesses as an apostle.

Answer built on scripture-blocks below

In the same way, the Spirit helps us in our weakness, for we do not know how we should pray, but the Spirit himself intercedes for us with inexpressible groanings. And he who searches hearts knows what is the mind of the Spirit, because the Spirit intercedes for the saints according to the will of God.

We [Christians] do not know how to pray as we ought.  Therefore, the Holy Spirit helps in this weakness by amending our prayers with “inexpressible groanings” that are deeper than [human] words. God, the Father, searches all hearts/minds of course knows what is the mind of the Spirit, because the Spirit is doing this intercession for the saints according to the will of God.

Paul emphasizes the Christian’s relationship to the Holy Spirit throughout the entire chapter for those who are “in Christ Jesus” (vs 1). Contrasting with the flesh, some of the points made about this relationship include:

  • the law of the life-giving Spirit set us free,
  • we are to walk according to the Spirit,
  • outlook should be shaped by the Spirit — an outlook that is life and peace and submitting to the law of God,
  • made alive by the Spirit living in us,
  • those led by the Spirit are sons of God.
Scripture-block application to this question

The Holy Spirit helps those “in Christ” to pray since they don’t know how to express the things needed spiritually.

!! scripture-block context extra important here !!

Therefore, one who speaks in a tongue should pray for the power to interpret. For if I pray in a tongue, my spirit prays but my mind is unfruitful. What am I to do? I will pray with my spirit, but I will pray with my mind also; I will sing praise with my spirit, but I will sing with my mind also.

Therefore, anyone with the gift of tongues should pray [to God] for the power to also interpret. For if I [Paul] pray in a tongue, my spirit is praying but my intellect isn’t benefiting.  What should I do then? I will pray with both my spirit and my mind, just as I will sing praises with my spirit and with understanding.

Paul is writing to the church in Corinth about orderly worship (really beginning all the way back in chapter 10). Beginning in chapter 12 and through this chapter 14, he is addressing speaking in tongues and mostly comparing/contrasting this gift of the Spirit and its appropriate use with the gift of prophesying.  In particular, they were using miraculous gifts of tongues improperly (with no interpreter – vs 27).  Since there was no interpreter, it was not useful for the “building up” of the church (vs 5), therefore it wasn’t to be done (without an interpreter).

Scripture-block application to this question

“Spirit” here is not referring to the Holy Spirit and therefore doesn’t apply to this question. His larger point is that no one should speak in a tongue without an interpreter and he’s applying it even to himself. To pray in the Spirit is not to pray in tongues.

!! scripture-block context extra important here !!

In all circumstances take up the shield of faith, with which you can extinguish all the flaming darts of the evil one; and take the helmet of salvation, and the sword of the Spirit, which is the word of God, praying at all times in the Spirit, with all prayer and supplication.

In all situations, take up the shield of faith which can put out all Satan’s flaming darts.  Put on the helmet of salvation and the sword of the Spirit which is the word of God, making sure to always offer prayer in the Spirit.

Paul’s metaphor of the Christian’s armor to be used in the spiritual battle that is waged.

Scripture-block application to this question

The Spirit equips the child of God with “armor” to fight off Satan. One of these weapons is our ability to pray in the Spirit.

It is these who cause divisions, worldly people, devoid of the Spirit. But you, beloved, building yourselves up in your most holy faith and praying in the Holy Spirit, keep yourselves in the love of God, waiting for the mercy of our Lord Jesus Christ that leads to eternal life.
It is worldly people that do not have the Spirit that cause divisions. But you, brethern, keep yourselves in fellowship with God until the coming of our Lord Jesus Christ leading to eternal life by building yourselves up in faith and praying in the Holy Spirit.

Jude’s letter to Christians warning them of false teachers that have “crept in unnoticed” (vs 4).

Scripture-block application to this question

Jude reminds those confronting false teaching that prayer in the Spirit will build up and help to keep one “in the love of God”.

The God of our fathers raised Jesus, whom you killed by hanging him on a tree. God exalted him at his right hand as Leader and Savior, to give repentance to Israel and forgiveness of sins. And we are witnesses to these things, and so is the Holy Spirit, whom God has given to those who obey him.

You [High Priest and Jewish Council] killed Jesus by hanging Him on a cross, but the God of our ancestors raised Him and exalted him at His right hand as Leader and Savior, thereby bringing Israel repentance and forgiveness of sins.  We [apostles], together with the Holy Spirit – who God, the Father, has given to all that obey Him – are witnesses to these things.

In the early days of the Christian movement and God’s establishment of His “new covenant,” the apostles are carrying the message of the gospel across Jerusalem and Judea.  Being confronted by the Jewish leadership (vs 27), as often they were, Peter tells them, “We must obey God rather than men” (vs 29) and witnesses to them about the things he and the others have seen with their eyes.  In this case, Peter may be specifically referring back to witnessing the transfiguration of Jesus documented in Acts 1.

Scripture-block application to this question

All believers are given the Holy Spirit, and thus are “in the Holy Spirit”.

If you then, who are evil, know how to give good gifts to your children, how much more will the heavenly Father give the Holy Spirit to those who ask him!

If you who are sinful know how to give good things to your children, how much more will your Father in heaven give the Holy Spirit to those that ask Him!

Jesus, in the midst of His public ministry, is presumably alone with His disciples. They have asked Him to teach them how to pray (vs 1).
Scripture-block application to this question

Jesus teaches how much the Father is willing to give to those that ask Him.

!! scripture-block context extra important here !!

Jesus is speaking to His disciples, therefore, those that are already believers and have been given the Holy Spirit in baptism5. Therefore, the giving is a further giving and guidance of the Holy Spirit for a believer.

I write these things to you who believe in the name of the Son of God that you may know that you have eternal life. And this is the confidence that we have toward him, that if we ask anything according to his will he hears us. And if we know that he hears us in whatever we ask, we know that we have the requests that we have asked of him.
I [John] am writing these things to those that already believe in the Son of God so that you may know that you have eternal life. Our confidence in God allows us to know He hears our prayers, and if we ask according to His will our requests are granted.

John is defining one’s love of God as the obedience (doing) of His word (vs 3).  Opposed to this is “the world” which stands in the way of a “victory” made possible by Jesus Christ (vss 4ff). John wants to remind brethren to remain strong and remember to pray to God for help (vs 13-16).

The pronoun “he” in vss 14-15 is qualified in vs 16 as God the father.

Scripture-block application to this question

There is no explicit mention of the Holy Spirit here, but John’s qualification that prayer requests be made “according to his will” certainly would qualify as “praying in the Spirit”.

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