The rift with his own conservative camp comes on top of the upheaval over Iran's disputed June 12 presidential election, which the opposition claims was rigged in Ahmadinejad's favour over challenger Mir Hossein Mousavi.
The president's latest troubles began earlier this month when he named a close associate, Esfandiar Rahim Mashaie, as his vice-president.
Rival politicians were angered because of past comments by Mashaie, who is the father-in-law of Ahmadinejad's son, that Iran's problems with Israel have nothing to do with the Israeli people or Jews in general.
|Ali Akbar Mehrabian's conviction is the latest embarrassment to ally Ahmadinejad [EPA]
Last week, Iran's supreme leader, Ayatollah Ali Khamenei, ordered Ahmadinejad to remove Mashaie.
The president stalled for days before finally conceding and accepting Mashaie's resignation on Friday, only to reappoint his as an adviser.
On Sunday, Ahmadinejad's office announced the dismissal of Gholam-Hossein Mohseni-Ejei, the intelligence minister.
No official reason was given for his sacking but the Mehr news agency quoted an unnamed source as saying that it was due to differences with Ahmadinejad over his decision to appoint Mashaie as first vice-president.
Ahmad Tavakkoli, a prominent conservative politician, criticised Ahmadinejad on Sunday for the intelligence minister's dismissal, saying that "there is no logical justification'' for it.
And Mohammad-Hossein Saffar-Harandi, the culture minister, quit on Sunday, citing "the recent events which shows the esteemed government's weakness".
Media reports spoke of an angry cabinet session and of two further ministers being fired as well, but Ahmadinejad's office said the reports of the dismissals were untrue.
The disputes are partly symbolic since Ahmadinejad is due to form a new government in August as he begins his second term as president.
But according to analysts, the rift could indicate that influential politicians are sensing weakness in the president amid the election dispute and are seeking to have greater control over him.
Ahmadinejad is scheduled to be sworn in as president on August 5 and introduce his new government members - which parliament must approve - by the end of the month.