Wright will leave his position after the Magpies' final-round match against Essendon at Windy Hill on Sunday, ending a three-season campaign.
The Magpies have managed just one win from 11 games to anchor the AFLW ladder alongside the Bombers and St Kilda.
The match will also be the last for Essendon coach Natalie Wood, while St Kilda are already looking for a replacement for Nick Dal Santo.
Wright's news comes after skipper Ruby Schleicher announced last week she would leave the Magpies to head home to Western Australia, with other players believed to be also planning a departure.
Tarni White, Lauren Butler, Bri Davey, Sarah Rowe and Mattea Breed are all out of contract, while vice-captain Jordyn Allen is contracted but is expected to seek other opportunities.
There's reportedly frustration among players and staff towards list management, development coaching and medical treatment at the powerhouse AFL club.
Wright backed Collingwood's commitment to the women's football program.
"I look forward to coaching the group this Sunday and I wish them all the very best for the future - I leave knowing Collingwood is committed to driving its AFLW program forward," he said in a statement on Tuesday.
"It has been a privilege to serve the AFLW program at Collingwood.
"I will always look back on my time at the Pies with gratitude, and I want to thank every player, coach, staff member and supporter I've shared this journey with.
"While these decisions are never easy, I know it is the right one for my family and the football program as we move forward."
The Magpies haven't made the AFLW finals since 2022 when they were semi-finalists, ending the season sixth.
Despite their resources, they have finished outside the top 10 in each of the following seasons.
20°C