Paula Sussex, chief executive of the Charity Commission, will leave the role later this year.
The regulator has today begun advertising for a successor to Sussex, who joined the commission in June 2014 after a career in the private sector.
A spokeswoman for the regulator said Sussex was appointed for a three-year term and had always said she would not want to extend her contract.
Sussex has agreed to stay for a few months beyond the end of June if necessary to ensure a smooth handover to her successor, the spokeswoman said.
The commission has been criticised repeatedly by the charity sector during Sussex’s time at the regulator.
In 2015, the charity leaders group Acevo accused the commission of having a "disproportionate focus" on Muslim charities after it opened a number of enquiries into Muslim charities over alleged links to extremist groups.
The commission’s decision to ask the Joseph Rowntree Charitable Trust to promise it would never again fund the advocacy group Cage, which was accused of having links with the alleged Islamic State killer known as Jihadi John, also drew criticism.
More recently, the commission’s proposal to charge charities for regulation has faced opposition.
However, it has also been praised by the National Audit Office for the progress made on achieving its targets.
In his introduction to the recruitment pack, William Shawcross, chair of the commission, says there has "never been a more exciting time to take this role, and we are looking for an exceptional person who will make the most of the opportunity".
He says the commission has made "huge progress" on its ambition to become a proactive, risk-based regulator.
The commission is looking for someone "who can pick up the baton from Paula without any loss of pace and develop the commission further as an agile and innovative organisation", says Shawcross.
"This is a high-profile position which requires a record of successful senior leadership and managing technology-enabled change in a complex environment," he writes.
"First-class communication skills, strong financial acumen and drive are also essential, together with the commitment, credibility and authority needed for this nationally important role."
The advert states a salary of about £130,000 a year for the role, which is in line with what Sussex has been receiving.