The vote was largely a formality after House Republicans nominated him for the position on Wednesday.
But even some conservatives who did not support Ryan said that after weeks of infighting, they were eager to move on and give Ryan the space to unite the party's various factions and craft a legislative agenda.
After losing 43 votes in the House GOP internal election a day earlier, only nine House Republicans voted against Ryan on the House floor.
Boehner gave a farewell address before the vote on Thursday, a day after the House approved a significant budget deal he negotiated with President Barack Obama and congressional Democrats. The legislation, which eliminates the possibility of a default and decreases the chance of a government shutdown, effectively gives Ryan a fresh start.
After he was sworn in as Speaker, Ryan praised Boehner, calling him "a true class act" and urged members from both sides to come together.
Ryan attempted to get members to turn the page saying "a lot is on our shoulders. So if you ever pray, pray for each other -- Republicans for Democrats, Democrats for Republicans."
After a standing ovation Ryan joked, "And I don't mean pray for a conversion."
He becomes the third Catholic in a row in the position, after Boehner and Nancy Pelosi, now the Minority Leader. He took the oath on his own copy of the New American bible and kept the gavel he wielded as Chairman of the powerful tax writing committee.
The 45-year-old Wisconsin Republican first worked on Capitol Hill as a legislative aide in 1992 and won his House seat in 1998 when he was 28.
Before officially handing him the gavel, Pelosi congratulated him and noted his path to the speakership went from serving as a young aide, and "a Tortilla Coast waiter," a restaurant just steps from the Capitol he will now preside over.
During his tenure in the House, Ryan became known as a policy wonk and attracted national attention for his sweeping proposals to overhaul Medicare and restructure the tax code. In 2012, Mitt Romney picked Ryan to be his running mate on the GOP ticket. After Republicans lost that election, he returned to the House and ruled out running for president in 2016, instead settling into what he called his "dream job" as chairman of the House tax writing committee.
Romney and his wife Ann were watching with Ryan's family inside the House chamber as he took the oath of office.
With the speaker's title, Ryan
takes on a national profile and the difficult challenge of corralling what has been an unruly and divided House GOP conference.
In his first speech he said the constant drama wasn't what the American people wanted and tried to move past it.
"We are not solving problems. We are adding to them. And I am not interested in laying blame. We are not settling scores. We are wiping the slate clean," Ryan said.
As he has been doing in the days leading up to Thursday's election, Ryan stressed he wanted members to have a greater imprint on legislation, and that he would empower committees and members with expertise to write bills instead of drafting them out of the Speaker's office.
"We will not always agree -- not all of us, not all of the time. But we should not hide our disagreements. We should embrace them. We have nothing to fear from honest differences honestly stated. If you have ideas, let's hear them."
After Ryan delivered his maiden speech as Speaker he walked down to shake hands with his colleagues, even with one who voted against him, still holding the Bible he placed his hand on to take the oath of office.