The historic encounter between the former IRA commander – now Northern Ireland's Deputy First Minister – and the Queen was unthinkable a little over 10 years ago.
But the success of the peace process and the Queen's acclaimed visit to the Republic Of Ireland last year, when her conciliatory words and gestures won over many critics of the monarchy, paved the way for their meeting.
The much-anticipated first handshake took place in a room within Belfast's Lyric theatre during an event celebrating the arts in the Republic and Northern Ireland.
Mr McGuinness was a senior member of the IRA when it killed the Queen's cousin Lord Mountbatten in a bomb blast in 1979.
The Queen is the head of Britain's Armed Forces, seen in the past by Republicans as occupying troops in Northern Ireland.
In a quiet space used by the Lyric for creative learning, the two met and were joined by the Duke Of Edinburgh, Northern Ireland First Minister Peter Robinson, Irish President Michael D Higgins and his wife Sabina.
The McGrath Suite is usually filled with toddlers enjoying story-telling sessions or drama students taking part in workshops.
But today it was sparsely furnished with leather seating – four chairs and a sofa – set around a circular wooden table decorated with flowers, with tea, coffee and still and sparkling water on a side table. The floor-to-ceiling windows looking out on to landscaped gardens and the River Lagan were covered with curtains.
The Queen later shook hands in public with Mr McGuinness in a gesture of reconciliation.
Mr McGuinness, as he held the monarch's hands for a few moments, spoke to her in Irish and told her the words meant: "Goodbye and God's speed."
Asked how David Cameron viewed the handshake, the Prime Minister's official spokesman said: "Clearly, there was a visit by Her Majesty to the Republic Of Ireland last year. That has taken relations between the two countries to a new level.
"We think it is right the Queen should meet representatives from all parts of the community."
The meeting with Mr McGuinness was separate to the Queen's two-day Diamond Jubilee visit to Northern Ireland, which yesterday saw her and Philip tour Enniskillen.