Cheap flights from Colorado to St. John's from $325

This is the cheapest one-way flight price found by a momondo user in the last 72 hours by searching for a flight from Colorado to St. John's departing on 5/30. Fares may change, and may not be available for all flights or travel dates. Click the price to refresh the search for this deal.
1 adult
1 adult, Economy, 0 bags

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Cheap round-trip flights

Enter your travel dates to find the best prices.
JetBlue Logo
11:59 pm - 12:52 pm
DEN
-
ANU
10h 53m
1 stop
JetBlue Logo
1:52 pm - 10:59 pm
ANU
-
DEN
11h 07m
1 stop
$588JetBlue
Sat, May 2 - Fri, May 8
JetBlue Logo
11:59 pm - 12:52 pm
DEN
-
ANU
10h 53m
1 stop
JetBlue Logo
1:52 pm - 10:59 pm
ANU
-
DEN
11h 07m
1 stop
$594JetBlue
Sun, May 3 - Mon, May 11
JetBlue Logo
11:59 pm - 12:52 pm
DEN
-
ANU
10h 53m
1 stop
JetBlue Logo
1:52 pm - 10:13 pm
ANU
-
DEN
34h 21m
2 stops
$620JetBlue
Sat, May 2 - Fri, May 8
JetBlue Logo
11:41 pm - 2:37 pm
DEN
-
ANU
12h 56m
1 stop
JetBlue Logo
3:42 pm - 12:08 pm
ANU
-
DEN
22h 26m
1 stop
$624JetBlue
Sat, May 23 - Sat, May 30
JetBlue Logo
11:59 pm - 12:47 pm
DEN
-
ANU
10h 48m
1 stop
JetBlue Logo
1:52 pm - 10:59 pm
ANU
-
DEN
11h 07m
1 stop
$650JetBlue
Fri, May 8 - Fri, May 15
JetBlue Logo
11:28 pm - 12:52 pm
DEN
-
ANU
35h 24m
2 stops
JetBlue Logo
1:52 pm - 10:13 pm
ANU
-
DEN
34h 21m
2 stops
$653JetBlue
Sat, May 2 - Fri, May 8
JetBlue Logo
11:59 pm - 12:54 pm
DEN
-
ANU
10h 55m
1 stop
JetBlue Logo
1:57 pm - 11:04 pm
ANU
-
DEN
11h 07m
1 stop
$668JetBlue
Thu, Apr 23 - Thu, Apr 30
JetBlue Logo
11:41 pm - 2:37 pm
DEN
-
ANU
12h 56m
1 stop
JetBlue Logo
3:42 pm - 12:08 pm
ANU
-
DEN
22h 26m
1 stop
$672JetBlue
Sat, May 23 - Sat, May 30
American Airlines Logo
11:41 am - 12:12 pm
DRO
-
ANU
22h 31m
2 stops
American Airlines Logo
3:25 pm - 11:11 am
ANU
-
DRO
21h 46m
2 stops
$974American Airlines
Sat, May 9 - Sat, May 16
American Airlines Logo
5:04 pm - 4:19 pm
DRO
-
ANU
21h 15m
2 stops
American Airlines Logo
5:20 pm - 4:34 pm
ANU
-
DRO
25h 14m
2 stops
$979American Airlines
Wed, May 6 - Wed, May 13

JetBlue flights from Colorado to St. John's, Saint John

Our best JetBlue deals on Colorado to St. John's, Saint John flight tickets
JetBlue
May 2
DEN11:59 pmDenver Intl
10h 53m
1 stop
ANU12:52 pmSt. John's V.C. Bird Intl
May 8
ANU1:52 pmSt. John's V.C. Bird Intl
11h 07m
1 stop
DEN10:59 pmDenver Intl
$588
JetBlue
May 3
DEN11:59 pmDenver Intl
10h 53m
1 stop
ANU12:52 pmSt. John's V.C. Bird Intl
May 11
ANU1:52 pmSt. John's V.C. Bird Intl
11h 07m
1 stop
DEN10:59 pmDenver Intl
$594
JetBlue
May 2
DEN11:59 pmDenver Intl
10h 53m
1 stop
ANU12:52 pmSt. John's V.C. Bird Intl
May 8
ANU1:52 pmSt. John's V.C. Bird Intl
34h 21m
2 stops
DEN10:13 pmDenver Intl
$620

American Airlines flights from Colorado to St. John's, Saint John

Our best American Airlines deals on Colorado to St. John's, Saint John flight tickets
American Airlines
May 26
DEN6:10 pmDenver Intl
20h 04m
2 stops
ANU4:14 pmSt. John's V.C. Bird Intl
Jun 1
ANU5:14 pmSt. John's V.C. Bird Intl
20h 35m
2 stops
DEN11:49 amDenver Intl
$775
American Airlines
Apr 26
DEN11:59 pmDenver Intl
14h 20m
2 stops
ANU4:19 pmSt. John's V.C. Bird Intl
May 3
ANU1:15 pmSt. John's V.C. Bird Intl
23h 24m
2 stops
DEN10:39 amDenver Intl
$780
American Airlines
Sep 4
DEN3:12 pmDenver Intl
20h 43m
2 stops
ANU1:55 pmSt. John's V.C. Bird Intl
Sep 12
ANU4:20 pmSt. John's V.C. Bird Intl
19h 40m
2 stops
DEN10:00 amDenver Intl
$785

momondo Fare Finder

 
Customize your flight search to find flights from Colorado to St. John's, Saint John that fit within your specific budget. Explore options based on user searches and filter the results based on your desired price range. Find flights that match your budget for a cost-effective journey. Over the last 7 days, momondo users made 832,500 searches. Data last updated March 29, 2026.
Use the filters below to find and compare flights from Colorado to St. John's, Saint John that are best for you.

Fly from

Fly to

Route

Depart

Return

Price

Cheapest round-trip

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/2

11:59 pm-12:52 pm

1 stop10h 53m

St. John's V.C. Bird Intl

Fri 5/8

1:52 pm-10:59 pm

1 stop11h 07m

$588

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sun 5/3

11:59 pm-12:52 pm

1 stop10h 53m

St. John's V.C. Bird Intl

Mon 5/11

1:52 pm-10:59 pm

1 stop11h 07m

$594

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/2

11:59 pm-12:52 pm

1 stop10h 53m

St. John's V.C. Bird Intl

Fri 5/8

1:52 pm-10:13 pm

2 stops34h 21m

$620

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/23

11:41 pm-2:37 pm

1 stop12h 56m

St. John's V.C. Bird Intl

Sat 5/30

3:42 pm-12:08 pm

1 stop22h 26m

$624
Quickest round-trip

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Fri 5/8

11:59 pm-12:47 pm

1 stop10h 48m

St. John's V.C. Bird Intl

Fri 5/15

1:52 pm-10:59 pm

1 stop11h 07m

$650

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/2

11:28 pm-12:52 pm

2 stops35h 24m

St. John's V.C. Bird Intl

Fri 5/8

1:52 pm-10:13 pm

2 stops34h 21m

$653

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 4/23

11:59 pm-12:54 pm

1 stop10h 55m

St. John's V.C. Bird Intl

Thu 4/30

1:57 pm-11:04 pm

1 stop11h 07m

$668

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 5/23

11:41 pm-2:37 pm

1 stop12h 56m

St. John's V.C. Bird Intl

Sat 5/30

3:42 pm-12:08 pm

1 stop22h 26m

$672

DurangoSt. John's

DRO - ANU

DROANU

Durango La Plata County

Sat 5/9

11:41 am-12:12 pm

2 stops22h 31m

St. John's V.C. Bird Intl

Sat 5/16

3:25 pm-11:11 am

2 stops21h 46m

$974

DurangoSt. John's

DRO - ANU

DROANU

Durango La Plata County

Wed 5/6

5:04 pm-4:19 pm

2 stops21h 15m

St. John's V.C. Bird Intl

Wed 5/13

5:20 pm-4:34 pm

2 stops25h 14m

$979

Flights are sorted by cheapest round-trip flights first.

Showing 1-10 of 20 resultsSorted by cheapest first
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See travel insights to St. John's from

How to get the cheapest flight ticket from Colorado to St. John's, Saint John

Look no further. We've gone through all the searches for this route on momondo so you have the important information and insights to find the cheapest flight ticket for your trip

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

The cheapest month to fly to St. John's, Saint John from Colorado is in February. Flight prices, which tend to average around $707, are often lower during this time because this is during the off-season. The month of January is another great option to travel to St. John's, Saint John, with average flight prices from Colorado averaging around $723.

Cheap Colorado to St. John's, Saint John flight deals and tips

Find info about flight duration, direct flights, and airports for your flight from Colorado to St. John's, Saint John

Fastest flight time

10h 39m

Direct flights

None
The fastest flight from Colorado to St. John's, Saint John takes 10h 39m
There are no direct flights from Colorado to St. John's, Saint John. There are no popular flight routes from Colorado to St. John's, Saint John.
  • When did momondo last update prices for flights from Colorado to St. John's V.C. Bird Intl Airport?

    Prices for flights from Colorado to St. John's V.C. Bird Intl Airport refresh daily.

  • How many operators does momondo search for flights from Colorado to St. John's V.C. Bird Intl Airport?

  • How old do you have to be to fly from Colorado to St. John's V.C. Bird Intl Airport?

    The minimum age for a child to fly alone is five, but airlines that offer an unaccompanied minor (UNMR) service may have their own age limitations. Flight duration, scheduling, and layovers are among the considerations that may influence age limits. We recommend that you double-check with the airline you are booking with for travel from Colorado to St. John's V.C. Bird Intl Airport.

  • What documentation or ID do you need to fly to St. John's V.C. Bird Intl Airport?

    The travel and health documents you'll need for your trip to St. John's V.C. Bird Intl Airport may differ based on your itinerary and personal situation. Typically, you should have several documents on hand, such as a national ID card or driver's license and a passport that is valid for six months after your intended arrival at St. John's V.C. Bird Intl Airport. It is always advisable to seek advice from your airline or a trusted third party, such as IATA.

Best airlines flying from Colorado to St. John's, Saint John

Compare and see reviews for airlines that fly from Colorado to St. John's, Saint John with momondo
Airline
Rating
Free Cancellation
Price
American AirlinesPriceFrom $698Free CancellationRating
7.1
11,521 reviews
Search American Airlines flights

Traveling to a place near St. John's?

Book flights to St. John's if you plan to visit one of these locations
Jolly Harbour
English Harbour
Falmouth

Why use momondo?

Why should I use momondo to find a flight deal from Colorado to St. John's?

momondo collates all your flight options in one place and lets you filter them to find the perfect flight from Colorado to St. John's. momondo saves you time and could save you money on your trip.

Can I find flights from Colorado to St. John's with flexible booking policies on momondo?

Flights from Colorado to St. John's with flexible booking policies can be found by using the search form above and then selecting our dedicated flexible booking filter, which will highlight only the flights where this policy is applied.

How can momondo help me find flights from Colorado to St. John's?

Once all potential Colorado to St. John's flight options are in front of you, momondo lets you sort and filter flights based on preferences such as airline, price and flight times amongst many other options.

I’m not ready to book a flight from Colorado to St. John's right now. Can momondo alert me if prices change?

Yes. momondo can track prices for Colorado to St. John's flights and alert you when they change. Perform a search to set up the price alert. All that is required is a valid email address.

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1 adult
Tue 4/28
Tue 5/5

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