The Chief Minister handed over his resignation to Manipur Governor Ajay Kumar Bhalla as the incumbent BJP government in the riot-hit state faces the possibility of a no-confidence motion and a floor test by the Congress-led Opposition.
"It has been an honour to serve the people of Manipur so far," Singh said in his letter which was submitted to the Governor at the Raj Bhavan in the presence of other BJP leaders and MLAs.
Biren Singh's resignation came soon after he met Union Home Minister Amit Shah in New Delhi and returned to Manipur.
The BJP has 32 MLAs in Manipur Assembly, along with additional support from five legislators of the Naga People's Front and six from the JD(U).
Despite the withdrawal of support by ally Conrad Sangma's National People's Party, the BJP maintains a comfortable majority. However, there was speculation that MLAs advocating for a leadership change in the state might have defied the party whip in the event of a floor test.
The Congress holds five seats in Manipur's 60-member Assembly, while the opposition National People's Party (NPP) has seven legislators. Additionally, there are three Independent MLAs and two members representing the Kuki People's Alliance.