The 28-year-old came through the Wednesday youth ranks and made 89 appearances between the sticks for his boyhood club. However, having been in and out of the Owls side, he left to join Derby permanently in 2022.
He made the number one shirt at Pride Park his own, helping the Rams clinch promotion to the Premier League in his second season at the club. He also scooped the League One Golden Glove, a just reward for his record of 20 clean sheets.
Derby have published a retained list following the conclusion of their campaign, confirming Wildsmith will be seeking pastures new this summer. He is leaving Derby with a total of 97 appearances for the club on his CV.
In a statement, Derby said: “Captain and midfielder Conor Hourihane is to depart after leading the side to promotion back to the Championship.
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“Striker Dwight Gayle, goalkeeper Scott Loach, midfielder Korey Smith, striker Martyn Waghorn and goalkeeper Joe Wildsmith are also moving on, leaving with the club’s very best wishes for the future.
“Forward Tom Barkhuizen and long-serving defender Craig Forsyth have activated performance-based clauses in their contracts to extend their stays with the club by an additional year.
“Midfielder Liam Thompson has had an option in his contract taken up for a further 12 months, while young midfielder Darren Robinson has signed a new two-year contract until 2026. Striker James Collins and Academy graduate Louie Sibley are in discussion with the club over their futures.”
Wildsmith also counts Barnsley among his former clubs, having had a brief loan spell at Oakwell in 2015.