Spooky was born Paul Miller in Washington, D.C. His father was a lawyer and member of the faculty at Howard University but died when Miller was only three. He inherited his father's record collection, which, along with frequent trips around the world (thanks to his mother's international fabric store), opened his eyes to a wide range of music. Growing up in the '80s saw Miller interested in D.C.'s hardcore punk scene and British ska-punk as well as go-go music. While attending college in Maine, Spooky began mixing on his own radio show and attempted to introduce his KRS-One tapes into classroom discussions on deconstruction (an idea made quite conceivable just ten years later). After graduating with degrees in French literature and philosophy, he moved to New York, where he wrote science fiction alongside advertising copy and pursued visual art as well. He was still into hip-hop, however, and formed the underground Soundlab collective (with We, Byzar, Sub Dub, and others), a scene that later morphed into the illbient movement.

After an assortment of singles and EPs during 1994-1995, Spooky gained a record contract from Asphodel in 1996 and released his debut album, Songs of a Dead Dreamer. The single "Galactic Funk" became a hit on the club scene, leading to recording appearances with Arto Lindsay and remixing spots for Metallica, Sublime, Nick Cave, and Spookey Ruben; Spooky also began writing regular journalist columns, for The Village Voice and Vibe. As if that didn't keep him busy, he also released the mix album Necropolis: The Dialogic Project, recorded a Paul D. Miller solo LP titled Viral Sonata, and performed in a new digital version of the Iannis Xenakis composition Kraanerg. His second proper album, 1998's Riddim Warfare, saw Spooky with a cast including disparate indie world figures from Dr. Octagon to Thurston Moore. He has also mounted visual exhibits at the Whitney Museum in New York and scored the award-winning 1998 film Slam.

One year later, he released File Under Futurism, a co-production with the Freight Elevator Quartet. 2000 saw the release of a collaborative effort with Scanner entitled The Quick and the Dead. The highly praised mix CD Under the Influence appeared the following year, but the next real album to appear from the DJ was 2002's Modern Mantra. That same year, as part of its Blue Series Continuum, Six Degrees released Optometry, a collaboration featuring Spooky with numerous progressive jazz artists such as William Parker and Matthew Shipp. Its remix companion, Dubtometry, appeared early in 2003. In 2004 Spooky teamed with the dub outfit Twilight Circus for Riddim Clash released by Play. The same year he was courted to remix two different label's output. A mix of Sub Rosa material appeared as Rhythm Science in January, and Thirsty Ear gave Spooky access to their Blue Series for Celestial Mechanix, released in June. In 2005, Drums of Death, a collaboration with Slayer and Fantômas drummer Dave Lombardo, came out, followed the next year by the DJ Spooky-curated collection 50,000 Volts of Trojan Records.

A year later the DJ remixed some favorites from the legendary reggae label's catalog on the fascinating album Creation Rebel. In 2008, Spooky edited Sound Unbound, a collection of essays on music and art. That same year, he made an appearance in FLicKeR, a documentary about the Dream Machine, an invention pioneered by Brion Gysin. In 2009, Miller issued The Secret Song, his first new studio release of original material in a decade. He collaborated with a slew of artists, including a jazz quartet, a chamber ensemble, pianist Vijay Iyer, various rappers including members of the Jungle Brothers, wordsmith Mike Ladd, and Sonic Youth's Thurston Moore. The disc was packaged with a DVD that included his soundtrack to a visual montage of two of the earliest films by Russian director Dziga Vertov.