Lee Collins, who was the captain of Yeovil Town, was 32.
The defender counted Wolves, Port Vale, Barnsley, Northampton, Mansfield and Forest Green as former club and had spent two years with the National League club in Somerset. His career also took in eight games on loan at Shrewsbury in 2012.
The club's National League fixture against Altrincham, which was due to be played on Friday, has been called off.
A club statement read: "All at Yeovil Town Football Club are mourning the loss of club captain Lee Collins.
"Lee sadly passed away yesterday and our thoughts and prayers go out to his family and friends.
"We ask everyone to respect the family's privacy at this time.
"The club will make no further comment at this time. Our game with Altrincham has been postponed."
Collins, who hails from Telford, began his career in the academy at Wolves but didn't make a first team appearance for the then-Championship club, instead moving to Hereford and Port Vale on loan.
He joined Port Vale permanently in 2008, playing 163 times for the League Two side, before moving on to Barnsley in 2011.
The centre-back made seven appearances for the Tykes before being sent out on loan to Shrewsbury Town.
He then moved on to Northampton Town, playing 86 times for the club, and moved on to Mansfield and Forest Green in League Two.
Shrewsbury Town issued a statement following the news, expressing their sadness.
"Shrewsbury Town is devastated to hear about the passing of former Town player, Lee Collins. Everyone at Shrewsbury Town sends our condolences to everyone at Yeovil Town as well as Lee's family and friends. Rest in peace." it read.
Wolves offered a statement of their own passing on their well wishes to Collins' friends and family.
"We offer our thoughts and love to all of Lee's friends and family following this unbelievably tragic news." the club said.
No details on the circumstances of his death have been revealed.