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elly Chambers has left Reading after 16 years with the club as player and manager "to pursue new opportunities".
The 37-year-old joined Reading as a player in 2007 and had served as manager since 2015 in her second spell in charge.
Reading were relegated from the Women's Super League in 2022-23 after eight years, and will switch to part-time for next season.
Chambers is expecting her second child this summer.
"I have made an extremely difficult decision to step away from the club that has been my life and become my family over the last 20 years," she Chambers said in a statement on Twitter.
"Thank you to the club for putting trust in me and giving me the platform to be able to build and achieve the things I have and make this team as successful as it could be."
Referring to the decision to go part-time, Reading said in a statement on their website: "Kelly consulted with the club at the start of that process and made clear her intentions to now pursue new opportunities.
"A player and a coach before becoming the manager and a valued and dedicated member of senior management within the structure of the club, Chambers has been a pioneer at the pinnacle of women's sport, championing women's football at every turn and standing strong at the very heart of its rapid growth.
"Everyone would like to thank Kelly for her remarkable contribution to Reading Football Club, wish her the very best of luck in her future career and offer our very best wishes to her and her family as she prepares for the arrival of her second child in the coming weeks."
After her playing career was ended by an anterior cruciate ligament injury, Chambers first took charge of Reading in 2012, before returning to the manager's seat three years later.
She guided them to the WSL that season, where they remained for eight campaigns.
Reading finished fourth in the top tier in 2017-18 - behind only Arsenal, Chelsea and Manchester City - and the following season reached the Women's FA Cup semi-final.
However, Reading, who were the only WSL side not affiliated with a Premier League team, were relegated on the final day of last season with defeat to champions Chelsea.
"I know last season didn't go the way we wanted it to and it is getting harder and harder to compete but please stick by this team," Chambers said.
"There are some unbelievable people working behind the scenes to make sure this team grows again, and they are going to need you and your support along the way.
"Once a royal, always a royal."
Chambers oversaw her 150th WSL game in January.
Emma Sanders, BBC Sport
This is a huge blow to Reading at a concerning time for the women's team following their relegation from the WSL and the move to a part-time model.
Chambers played a vital role in building a club structure, providing opportunities for youth development and setting up a professional first team in her many roles across the last two decades.
During her time at Reading she became a figure of hope, guiding the team to WSL safety on numerous occasions when they were battling against clubs with bigger financial sway.
She was in tears as Reading's eventual relegation was confirmed on the final day of this season and many feared then she would be considering her future.
With the club reverting to part-time status, it felt only a matter of time before Chambers' departure was confirmed because she has proven her worth as a WSL manager on several occasions and is held in high respect among those in the game.
It is understood West Ham, who are seeking a new manager, have reached out to Chambers to express their interest, while Tottenham and Women's Championship club Crystal Palace are also on the lookout for a head coach.
Chambers is due to give birth any day now, but she took just two weeks off work last time and could do the same again.
First-team coach Phil Cousins, who has worked alongside Chambers in the WSL, is said to be favourite to take over at Reading on an interim basis, at least for the summer, while they look to build a squad to compete in the Championship.
