The father-of-three, who was four days short of his 37th birthday, also played for Celtic and Manchester United during an illustrious career, which took him to five countries and saw him represent his country on 21 occasions.
He was diagnosed with pancreatic cancer last year and returned to Cork in November for treatment at Marymount.
President Michael D Higgins led the tributes to Miller. He said, "It is with great sadness that I learned of the death of Liam Miller, who brought skill and passion to his games, for the Republic of Ireland, Cork City, Celtic, Manchester Utd. and other clubs. I send my condolences to his family and friends, and all those who love Irish sport.”
Fellow pros and former teammates have also paid tribute to the Ovens man, who began his career with Celtic, before spending two seasons at Manchester United.
He also had spells at Leeds United, Sunderland - where he helped Roy Keane's team win promotion to the Premier League - and QPR and Hibernian.
A statement issued by Manchester United said, "Manchester United is deeply saddened to learn of the tragic death of our former midfielder Liam Miller. We extend our condolences to his loved ones at this extremely difficult time."
Miller's former clubs Celtic and Melbourne City both confirmed tributes to the Corkman this weekend, with a minute's silence and black armbands planned.
Dozens of Miller's former teammates have also paid tribute.
Ex-international teammate Kevin Kilbane said, “Sad hearing the awful news Liam has passed away, taken far too soon by a terrible disease. Proud to have shared a dressing room with him over the years.”
Kevin Doyle, who also played with Miller for the Republic of Ireland, described him as “a gentleman."
Former Celtic star John Hartson, who himself battled cancer, tweeted his condolences, adding, "Rest in peace young man."
Since 2016, Liam had lived in the United States with his wife and children, where he played with Wilmington Hammerheads, before moving on to a coaching role with Real Monarchs. The US club said: “We were heartbroken to hear of Liam’s passing. We admired his love of the game, his competitive spirit and his hard-working mentality.”
A statement from Cork Schoolboy League said their thoughts and prayers were with Liam’s family. A minute’s silence will be observed before all CSL games this weekend.