What are the cheapest airlines to fly from Colorado to St. John's, Saint John one-way?

For one-way options, check prices for JetBlue. According to our data, you can fly for as low as $368. Users have also found prices from $383 and $408 on American Airlines and Delta, respectively.

What are the most popular routes from Colorado to St. John's, Saint John?

The most popular flight routes from Colorado to St. John's, Saint John are Denver Intl - St. John's V.C. Bird Intl, Grand Junction Regnl - St. John's V.C. Bird Intl and Montrose County - St. John's V.C. Bird Intl.

How far in advance should I book a flight from Colorado to St. John's, Saint John?

Find a great deal and save up to 167% by booking at least 28 days prior to your desired departure date, rather than waiting until the week of travel. According to our data, there are a number of flights available from Colorado to St. John's, Saint John within the next two weeks, with the cheapest ticket starting at $575.

What is the cheapest month to fly from Colorado to St. John's, Saint John?

Our data shows that November tends to be the cheapest month to fly to St. John's, Saint John from Colorado. Users have commonly found prices around $793 for the month, but tickets can be as low as $487. Due to multiple factors, prepare for potentially higher prices in December.

What airport do you fly into for flights to St. John's from Colorado?

If you book a flight to St. John's from Colorado, you will be flying to V.C. Bird Intl, which is the city’s only airport. St. John's V.C. Bird Intl (ANU) is located 3.8 mi from the center of St. John's.

Can I find deals for flights from Colorado to St. John's that include hotel bookings?

Yes. In addition to deals on Colorado to St. John's flights, Cheapflights offers vacation packages that include both flights and hotel.

How can I find direct flights from Colorado to St. John's?

After entering your origin and destination, apply the non-stop filter on the search result page to find direct flights from Colorado to St. John's.

Can I find deals for business class flights from Colorado to St. John's?

Yes. Cheapflights offers flight deals from Colorado to St. John's by cabin class. In addition to browsing deals, you can also filter by cabin class on the search results page after making a search.

$368+ Flights from Colorado to St. John's

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Cheap flight deals from Colorado to St. John's

Most accurate provider	FlightHub 3 stars
Most trusted provider	FlightHub 3 stars
Round-trip from	$724 (American Airlines)
One-way from	$368 (JetBlue Airways)
Popular in	December
Cheapest in	November
Average price	$804

Provider with most accurate pricing for Denver Intl-St. John's V.C. Bird Intl flight deals.

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Provider most trusted by Cheapflights users for Denver Intl-St. John's V.C. Bird Intl flights.

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From Colorado to St. John's V.C. Bird Intl

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One-way flight from Colorado to St. John's V.C. Bird Intl

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High demand for flights, 0% potential price rise

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Cheapest flight prices on average. 3% potential price decrease ($25 potential savings vs. average RT price).

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Average for round-trip flights in April 2025

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Find flight deals from Colorado to St. John's

Cheapest flights from Colorado to St. John's
Explore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on April 2, 2025.

Sat 5/3111:53 pmDEN - ANU

1 stop13h 56mAmerican Airlines

Sat 6/71:45 pmANU - DEN

1 stop10h 55mAmerican Airlines

Deal found 4/1

$724

Fri 11/2811:25 amDEN - ANU

2 stops25h 20mMultiple Airlines

Sat 12/65:10 pmANU - DEN

3 stops25h 46mMultiple Airlines

Deal found 4/1

$2,213

Best flights from Colorado to St. John's
Discover carefully curated flight deals from Colorado to St. John's that have cost, travel time, and layovers in mind to ensure you get the best travel experience. Data last updated April 2, 2025.

Sat 5/3111:53 pmDEN - ANU

1 stop13h 56mAmerican Airlines

Sat 6/71:45 pmANU - DEN

1 stop10h 55mAmerican Airlines

Deal found 4/1

$724

Last-minute flights from Colorado to St. John's
Discover last-minute flight deals from Colorado to St. John's. Data last updated April 2, 2025 and is based on user searches.

Sat 5/3111:53 pmDEN - ANU

1 stop13h 56mAmerican Airlines

Sat 6/71:45 pmANU - DEN

1 stop10h 55mAmerican Airlines

Deal found 4/1

$724

One-way flights from Colorado to St. John's
Search for one-way flight options from Colorado to St. John's. Find affordable one-way fares based on user searches. Data last updated April 2, 2025.

Sat 5/1711:59 pmDEN - ANU

1 stop12h 12mJetBlue

Deal found 4/1

$368

Sat 5/176:46 pmDEN - ANU

2 stops15h 38mAmerican Airlines

Deal found 4/2

$383

Fri 5/1612:59 amDEN - ANU

1 stop11h 16mDelta

Deal found 4/2

$408

Cheapflights Fare Finder

Use the filters below to find and compare flights from Colorado to St. John's that are best for you.

Fly from

Fly to

Route

Depart

Return

Price

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/31

11:53 pm-3:49 pm

1 stop13h 56m

St. John's V.C. Bird Intl

Sat 6/7

1:45 pm-10:40 pm

1 stop10h 55m

$724

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/17

11:59 pm-2:11 pm

1 stop12h 12m

$368

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/17

6:46 pm-12:24 pm

2 stops15h 38m

$383

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Fri 5/16

12:59 am-2:15 pm

1 stop11h 16m

$408

Flights are sorted by cheapest round-trip flights first.

Deals found on 4/1

Best time to book a flight from Colorado to St. John's

Have a flexible travel schedule? Discover the best time to fly to St. John's from Colorado with our price prediction graph.

Estimated round-trip price

Rates are based on past data. Find the cheapest month and day to book your flight based on your travel requirements, then search for cheap deals.

Cheapflights Insights

Everything you need to know about your flight from Colorado to St. John's

What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

Currently, August is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $500). Flying from Colorado to St. John's, Saint John in June is currently the most expensive (average of $651). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

What is the cheapest time of day to fly from CO to ANU?

When flying from Colorado to St. John's, Saint John, the time of day you decide to fly out makes little to no difference towards the overall price you’ll pay on tickets.

Reviews of airlines servicing St. John's

Delta

8.0

Very good

7,898 reviews

Reviews

1 / 20

10.0

Excellent

Aaron,Oct 2024

LAX - LHR

This was a flight operated by Virgin Atlantic in their Upper Class cabin. Overall, an outstanding experience.

Delta

8.0

Very good

7,898 reviews

Delta

8.0

Very good

7,898 reviews

Reviews

1 / 20

10.0

Excellent

Aaron,Oct 2024

LAX - LHR

This was a flight operated by Virgin Atlantic in their Upper Class cabin. Overall, an outstanding experience.

JetBlue

7.3

Good

2,922 reviews

Delta

8.0

Very good

7,898 reviews

Reviews

1 / 20

10.0

Excellent

Aaron,Oct 2024

LAX - LHR

This was a flight operated by Virgin Atlantic in their Upper Class cabin. Overall, an outstanding experience.

American Airlines

7.2

Good

10,000 reviews

Delta

8.0

Very good

7,898 reviews

Reviews

1 / 20

10.0

Excellent

Aaron,Oct 2024

LAX - LHR

This was a flight operated by Virgin Atlantic in their Upper Class cabin. Overall, an outstanding experience.

Related info for your journey

What airport do you fly into for flights to St. John's from Colorado?
If you book a flight to St. John's from Colorado, you will be flying to V.C. Bird Intl, which is the city’s only airport. St. John's V.C. Bird Intl (ANU) is located 3.8 mi from the center of St. John's.
What are the cheapest airlines to fly from Colorado to St. John's, Saint John one-way?
For one-way options, check prices for JetBlue. According to our data, you can fly for as low as $368. Users have also found prices from $383 and $408 on American Airlines and Delta, respectively.
What are the most popular routes from Colorado to St. John's, Saint John?
The most popular flight routes from Colorado to St. John's, Saint John are Denver Intl - St. John's V.C. Bird Intl, Grand Junction Regnl - St. John's V.C. Bird Intl and Montrose County - St. John's V.C. Bird Intl.
Can I find deals for flights from Colorado to St. John's that include hotel bookings?
Yes. In addition to deals on Colorado to St. John's flights, Cheapflights offers vacation packages that include both flights and hotel.
How can I find direct flights from Colorado to St. John's?
After entering your origin and destination, apply the non-stop filter on the search result page to find direct flights from Colorado to St. John's.
Can I find deals for business class flights from Colorado to St. John's?
Yes. Cheapflights offers flight deals from Colorado to St. John's by cabin class. In addition to browsing deals, you can also filter by cabin class on the search results page after making a search.
What is the cheapest month to book a flight from Colorado to St. John's, Saint John?
Currently, August is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $500). Flying from Colorado to St. John's, Saint John in June is currently the most expensive (average of $651). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

See more FAQs

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Top 2 airlines flying from Colorado to St. John's

Airline	Cheapest	Average	Flexibility	On-time
American Airlines	Cheapest$505	Average$781	FlexibilityNo cancel fee	On-time71%
JetBlue	Cheapest$519	Average$679	FlexibilityNo cancel fee	On-time62%

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$368+ Cheap flights from Colorado to St. John's (ANU)

This is the cheapest one-way flight price found by a Cheapflights user in the last 72 hours by searching for a flight departing on 5/17. Fares are subject to change and may not be available on all flights or dates of travel.

Find cheap flights from Colorado to St. John's with Cheapflights

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Cheap flight deals from Colorado to St. John's

Keep the following information in mind while searching for Colorado to St. John's flight deals. Data was last updated April 2, 2025.

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Most trusted provider

Round-trip from

One-way from

Popular in

Cheapest in

Average price

Find flight deals from Colorado to St. John's

Cheapest flights from Colorado to St. John'sExplore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on April 2, 2025.

Explore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on April 2, 2025.

Cheapflights Fare Finder

Use the filters below to find and compare flights from Colorado to St. John's that are best for you.

Best time to book a flight from Colorado to St. John's

Have a flexible travel schedule? Discover the best time to fly to St. John's from Colorado with our price prediction graph.

Cheapflights Insights

Everything you need to know about your flight from Colorado to St. John's

What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

What is the cheapest time of day to fly from CO to ANU?

Find hourly flight availability from Colorado to St. John's. Discover flight options and departure times throughout the day, allowing you to choose a departure time that suits your schedule. Data last updated April 2, 2025.

Reviews of airlines servicing St. John's

Related info for your journey

Find useful and relevant information for your journey from Colorado to St. John's. Access travel guides, tips, and recommendations to enhance your travel experience. Get information about local attractions, weather, transportation options, and more.

What airport do you fly into for flights to St. John's from Colorado?

What are the cheapest airlines to fly from Colorado to St. John's, Saint John one-way?

What are the most popular routes from Colorado to St. John's, Saint John?

Can I find deals for flights from Colorado to St. John's that include hotel bookings?

How can I find direct flights from Colorado to St. John's?

Can I find deals for business class flights from Colorado to St. John's?

What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

Browse thousands of different options on Cheapflights for your next trip

Toggle through the tabs below to find thousands of options on Cheapflights for your next trip.

Alternative routes for Colorado to St. John's

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Top 2 airlines flying from Colorado to St. John's

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Cheapest flights from Colorado to St. John's
Explore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on April 2, 2025.