O'Neill joined the Colorado Rapids youth system in 2009. He led the Rapids U18 team in scoring in 2011–12 with 10 goals in 15 games, helping them reach the playoffs. Professional
O'Neill originally signed to play college soccer at the University of Virginia, however on June 19, 2012, O'Neill signed with the Colorado Rapids as a Home Grown Player.
Three months later, he made his professional debut in a 3–0 victory over the Portland Timbers. His first career goal was May 24 of the same year. On August 7, 2015, O'Neill was acquired from Colorado by Cyprus club Apollon Limassol for an undisclosed amount of money.
However, Royal Mouscron-Péruwelz announced on their website that they had signed O'Neill on August 31, 2015. O'Neill's loan was cut short on the 23rd December 2015, and he returned to Limassol having not made an appearance for the Belgian club. International
O'Neill is eligible to represent both the United States and the Republic of Ireland.
On October 9, 2012, O'Neill was called up by the United States U20 national team for the 2012 Marbella Cup in Spain. A day later, O'Neill made his debut for the U20's in a 2–1 loss to Canada, however he suffered an eye injury that ruled him out for the rest of the tournament. He later played for the US at the 2013 FIFA U-20 World Cup.
He has yet to debut for the US senior team and has indicated a willingness to accept a call for his native Ireland. He participated in a US camp in January 2014, although he was dropped prior to a friendly against South Korea. He was called up to the United States senior squad for a friendly against Panama in February 2015.
O'Neill is the son of former All-Ireland winning Cork gaelic football player, Colm O'Neill, and is a nephew of former Kerry gaelic football player, Maurice Fitzgerald.