Jay DeMarcus was born in Columbus, Ohio. He attended Lee College where he was discovered and co-founded the contemporary Christian music group East to West and moved to Nashville, Tennessee in 1993. In 1999, Jay, along with his second cousin Gary LeVox, and guitarist, Joe Don Rooney, formed the country band, Rascal Flatts.

From 2000 to 2010, they recorded for Disney Music Group's Lyric Street Records. While on that label, they released seven albums, all of which have been certified platinum or higher by the Recording Industry Association of America (RIAA). After Lyric Street closed in 2010, they moved to Big Machine Records, for which they have released five albums. Their studio albums have accounted for more than 25 singles, of which 14 have reached No. 1 on Billboard Hot Country Songs and/or Country Airplay. Their longest-lasting No. 1 single, "Bless the Broken Road", spent five weeks in that position in 2005. In 2005–06, "What Hurts the Most" was No. 1 on both the Hot Country Songsand Adult Contemporary charts, and peaked at No. 6 on the Billboard Hot 100.

DeMarcus has co-produced albums for several artists, including Chely Wright's 2002 album Never Love You Enough, Chicago's Chicago XXX, and James Otto's 2008 album Sunset Man. He also produced New to This Town, the first solo album released by Kix Brooks and Jason Scheff's solo album, Here I Am. Grammy award winning albums: Jason Crabb's Love Is Stronger and Reba McEntire's Sing It Now Songs of Hope & Faith.

In October of 2018, DeMarcus founded the label Red Street Records, an independent Christian music label.