The mammalian genome is highly organized into 3D structures, including nuclear bodies for RNA processing. For example, highly transcribed RNAPII genes organize around nuclear speckles for pre-mRNA splicing. While it is known that speckle proximity is correlated with transcription level, whether active RNAPII transcription plays a mechanistic role in organization around speckles is less clear. Specifically, whether transcription drives localization to speckles (function promotes form) or whether speckles enhance transcription (form promotes function) is unknown. To explore this, we treated cells with Flavopiridol, a selective RNAPII elongation inhibitor, and measured RNA/DNA organization using RD SPRITE. We find that inhibition leads to a global reorganization of splicing components, with depletion of diffusible snRNAs from DNA and accumulation into larger speckle structures. Furthermore, we detect a loss of DNA organization around speckles, with previously active genes dissociating. This indicates that transcription is required for spliceosome recruitment to DNA and suggests that splicing factors are not released from speckles before gene activation. In addition, this demonstrates that active transcription is required for DNA organization around speckles and suggests that genes do not localize to speckles prior to activation, nor are high transcription levels simply due to speckle proximity. Together, these data support a coalescence model for how transcription and splicing factor binding are coupled to produce the structure and function of speckles: transcriptional levels increase spliceosome concentration at active DNA regions, which relocate closer to speckles; the result is highly transcribed regions with the highest spatial concentration of splicing factors arranged around speckles. Overall, our findings establish RNAPII transcription as a mediator of nuclear structure genome-wide and highlight the role for nascent RNA as a driver of nuclear organization.