Philip Hammond's two-day trip comes five weeks after Britain and five other world powers struck a deal with Iran to end a 13-year dispute over the Islamic republic's nuclear programme.
He led a ceremony in the embassy garden with Ajay Sharma, the new charge d'affaires who will represent Britain in Tehran, where the British flag was raised.
But the opening did not pass without incident as reporters spotted a "Death to England" slogan still scrawled in red paint on a door at the embassy residence.
Iran's embassy in London also reopened today. The two nations are expected to appoint ambassadors within months.
Hammond, the first British foreign secretary to visit Iran since Jack Straw in 2003, described the violence in 2011 as "a low point" but said a new journey was beginning.
"Over the coming months, we will work to ensure that the nuclear agreement is a success, including by making sure that it is fully implemented by all sides," he said at the reopening.
He later held a press conference with Mohammad Javad Zarif, Iran's foreign minister and lead negotiator in the near two years of nuclear talks that have ended Tehran's isolation from the West.
"We have come a long way but let's walk first and try to run later," Hammond said, again noting that bringing the nuclear deal into force and building confidence was the priority.
"It will be a process of evolution to overcome the deficit of trust."
"This region is faced with serious problems," he said alluding to the spread of the Islamic State jihadist group in Syria and Iraq.
"This requires a different approach. Iran is prepared to engage with all our neighbours. We need to start cooperation, not on a zero sum game but for mutual gain.
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