While “praying in the Spirit” may evoke “charismatic” prayer, this paper argues that from a scriptural point of view it defines all Christian prayer as having the Holy Spirit as main subject, who leads us to pray and prays in us, by showing us to whom, how and for what we should pray. This has implications for spirituality and pneumatology. On the one hand, prayer is to be understood as much more than the extension of our human desire towards God: it means entering into the divine will, the divine life, and the relations between Father, Son and Spirit – and relating to each in a different way. This actually helps to catch the essence of charismatic prayer as well, which is precisely letting the Spirit pray in us: charisms and “enthusiasm” are an expression of this and are in their right place when they are referred to it. On the other hand, the Holy Spirit manifests itself as a unique type of divine person, which acts and speaks in and through others. The paper contends that this economical specificity needs to be re-elaborated on the level of the immanent Trinity in a novel way: the divine names of Ruah and Pneuma allow us to conceive the Spirit as the most intimate Breath which the Father breathes (spires) into the depths of the Son.