"The totalitarian and arrogant leaders of the United States must know that their attempt to create divisions between the people and the political and military authorities in our country is a desperate and fruitless attempt," Foreign Ministry spokesman Bahram Qassemi said Thursday.
The official was apparently referring to Tillerson's Wednesday remarks in New Delhi that Washington's "fight is not with the Iranian people," but with what he described as "the revolutionary regime."
"We know there are strong feelings and values inside of Iran that we want to promote in terms of one day the Iranian people being able to retake control of their government," the top US diplomat said.
Qassemi said Tillerson's remarks "once again depicted the true face of the United States for the Iranian people."
Iranians got furious this month after US President Donald Trump called the country a "terrorist nation" and used "Arabian Gulf" to refer to the body of waters which is internationally known as the Persian Gulf.
The outrageous remarks prompted Iranians of all stripes to take to social media and state that they were united in defending their country after Trump refused to certify a landmark nuclear agreement and hinted at consequences.
Qassemi hit out at contradictory postures of US leaders, saying their "only consequence is strengthening solidarity and national unity and increasing hatred and abhorrence of the policies of the ignorant American statesmen."
He also touched on the history of Washington's enmity with Iran even when the country was a close ally of the United States before the Islamic Revolution in 1979, including its role in a coup which brought down Iranian Prime Minister Muhammad Mossadegh.
"American statesmen, who through the 1953 coup against a legitimate government and then an all-out support for the dictatorial regime of the Shah, were an accomplice to that regime's crimes have committed the most crimes against our people under the guise of supporting the Iranian people since the beginning of the Islamic Revolution."
Washington supported the former Iraqi dictator Saddam Hussein in his eight-year war against Iran in the 1980s, providing him with vital intelligence and weapons. The war also marked direct US attacks on Iran's offshore oil facilities in the Persian Gulf and downing of an Iranian Airbus in which 290 people were killed.
Earlier this week, Trump unveiled tougher immigration measures against Iranians along with the citizens of 10 other countries. Those measures were purportedly aimed at protecting Americans from possible terrorist attacks.
No Iranian has ever been implicated in any known terrorist attack but Saudi Arabia where 15 of the 19 terrorists involved in the September 11 attacks came from is not in the list.
The US and Iran have held no diplomatic relations since the Islamic Revolution and Qassemi on Thursday summed up some of Washington's hostile moves against Iran.
"The creation of unrest and chaos inside the country, attempts to carry out a coup, military, economic, political, logistical and intelligence support of the despotic and criminal regime of Saddam in his aggressive war and the imposition of illegal sanctions against the great people of Iran are only a small and insignificant part of America's interventionist moves over the past nearly 40 years."
On Wednesday, Iran's Foreign Minister Mohammad Javad Zarif also took aim at Tillerson's remarks, saying Iranians would not be fooled by US plots.
“US changed one elected govt in Iran— in 1953. It has tried a repeat since 79. Iranians not fooled by US game & unmoved by fake sympathy,” he tweeted.