The four reportedly quit over differences with the government on how to handle the deteriorating security situation that has seen attacks from Daesh and the Taliban escalate.
Afghanistan's ministers of defence and interior, as well as the spy chief, quit on Saturday, government sources said, following the resignation of the president's national security adviser earlier in the day.
"We have received four resignations by two ministers and two senior security officials," an official in President Ashraf Ghani's office said.
Government sources said the new resignations were from Defence Minister Tariq Shah Bahrami and Interior Minister Wais Barmak, as well as Masoom Stanekzai, the head of the National Directorate of Security. They followed a decision by National Security Advisor Hanif Atmar to quit.
Officials working directly with the two ministers and Stanekzai were not immediately available to comment.
But two senior interior ministry officials said the country's top security officials cited differences with the government over policy amid the deteriorating security situation as the main reason for resigning.
Heavy fighting between Taliban insurgents and Afghan forces across the country this year, as well as repeated suicide attacks in Kabul and other major cities, have underlined the dire security situation facing Afghanistan.
With parliamentary elections due on October 20, authorities had been bracing for more attacks. But even so, the scale of the violence has shocked government officials, who are facing bitter criticism over their handling of the war.
Afghan media outlet Tolo News director Lotfullah Najafizada speaks to TRT World about the impact of these resignations.
Ghani accepted the resignation of Atmar, and replaced him with Afghan Ambassador to the US Hamdullah Mohib.
Mohib also served as the non-resident ambassador to Mexico, the Dominican Republic, Argentina and Columbia.
Atmar had previously served as the interior minister under the former president, Hamid Karzai, after previous posts as minister of rural development and education.
Ghani rejected on Sunday resignations tendered a day earlier by three senior security officials, the government said.
The ministers of defence and interior, as well as intelligence chief, sent their resignations to the president's palace on Saturday, soon after Afghanistan's national security adviser also resigned.
Government spokesman Haroon Chakansuri said in a statement Ghani had asked the three officials to continue with their duties and "work towards the betterment of the security situation."