St. Johns County Homes With Guest House

Interested in the extra living space homes with a guest house provide? Featured here are all St. Johns County homes for sale with a guest house. If you’re interested in any of the St. John's County guest house home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest house.

And if you'd like to stay up-to-date on St. John's County homes with a guest house, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. Johns County Homes With Guest House

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New
135 Marine St, ST AUGUSTINE

$5,999,000

135 Marine St, ST AUGUSTINE

4 Beds 6 Baths 5,692 SqFt Residential MLS® # 1229284
New Pending
623 Saint Kitts Loop, ST AUGUSTINE

$725,000

623 Saint Kitts Loop, ST AUGUSTINE

5 Beds 4 Baths 3,165 SqFt Residential MLS® # 1228905
New
503 Arricola Ave, ST AUGUSTINE

$799,000

503 Arricola Ave, ST AUGUSTINE

3 Beds 3 Baths 1,908 SqFt Residential MLS® # 1228437
New
129 Hedgewood Dr, ST AUGUSTINE

$399,900

129 Hedgewood Dr, ST AUGUSTINE

3 Beds 4 Baths 2,162 SqFt Residential MLS® # 1228647
New
473 S Roscoe Ext Blvd, PONTE VEDRA BEACH

$1,100,000

473 S Roscoe Ext Blvd, PONTE VEDRA BEACH

3 Beds 4 Baths 3,375 SqFt Residential MLS® # 1228467
70 Weeden St, ST AUGUSTINE

$875,000

70 Weeden St, ST AUGUSTINE

2 Beds 2 Baths 1,443 SqFt Residential MLS® # 1227709
36 Colony St, ST AUGUSTINE

$1,300,000

36 Colony St, ST AUGUSTINE

4 Beds 4 Baths 3,295 SqFt Residential MLS® # 1227526
434 Ocean Forest Dr, ST AUGUSTINE

$3,795,000

434 Ocean Forest Dr, ST AUGUSTINE

4 Beds 4 Baths 7,321 SqFt Residential MLS® # 1226869
3075 Joe Ashton Rd, ST AUGUSTINE

$1,825,000

3075 Joe Ashton Rd, ST AUGUSTINE

3 Beds 2 Baths 1,152 SqFt Residential MLS® # 1226851
70 Coquina Ave, ST AUGUSTINE

$685,000

↓ $6,165,000

70 Coquina Ave, ST AUGUSTINE

2 Beds 1 Bath 1,602 SqFt Residential MLS® # 1226767
113 Cannon Ct W, PONTE VEDRA BEACH

$1,899,000

113 Cannon Ct W, PONTE VEDRA BEACH

5 Beds 6 Baths 3,827 SqFt Residential MLS® # 1223494
13745 County Road 13 N, ST AUGUSTINE

$825,000

13745 County Road 13 N, ST AUGUSTINE

5 Beds 3 Baths 2,423 SqFt Residential MLS® # 1225983
8165 A1a S, ST AUGUSTINE

$2,625,000

8165 A1a S, ST AUGUSTINE

6 Beds 6 Baths 5,623 SqFt Residential MLS® # 1225035
941 N Griffin Shores Dr, ST AUGUSTINE

$2,985,000

941 N Griffin Shores Dr, ST AUGUSTINE

4 Beds 4 Baths 4,608 SqFt Residential MLS® # 1224675
Under Contract
404 Old Quarry Rd, ST AUGUSTINE

$2,850,000

404 Old Quarry Rd, ST AUGUSTINE

4 Beds 4 Baths 3,699 SqFt Residential MLS® # 1223662
150 Mc Heather Ln, HASTINGS

$899,000

↓ $116,000

150 Mc Heather Ln, HASTINGS

4 Beds 4 Baths 2,427 SqFt Residential MLS® # 1223474
969 Ponte Vedra Blvd, PONTE VEDRA BEACH

$8,750,000

969 Ponte Vedra Blvd, PONTE VEDRA BEACH

4 Beds 6 Baths 8,277 SqFt Residential MLS® # 1219941
1524 Drury Ct, ST AUGUSTINE

$869,000

↓ $6,000

1524 Drury Ct, ST AUGUSTINE

5 Beds 4 Baths 3,005 SqFt Residential MLS® # 1221923
Pending
6595 Collier Rd, ST AUGUSTINE

$1,600,000

6595 Collier Rd, ST AUGUSTINE

5 Beds 5 Baths 5,407 SqFt Residential MLS® # 1219861
105 Plantation Cir S, PONTE VEDRA BEACH

$2,650,000

105 Plantation Cir S, PONTE VEDRA BEACH

4 Beds 5 Baths 4,764 SqFt Residential MLS® # 1217632
Under Contract
3329 State Rd 13 Rd N, ST JOHNS

$1,195,000

3329 State Rd 13 Rd N, ST JOHNS

4 Beds 3 Baths 4,222 SqFt Residential MLS® # 1216865
35 Atlantic Ave, ST AUGUSTINE

$799,999

↓ $65,001

35 Atlantic Ave, ST AUGUSTINE

4 Beds 4 Baths 2,430 SqFt Residential MLS® # 1214055
290 St George St, ST AUGUSTINE

$2,599,000

↓ $251,000

290 St George St, ST AUGUSTINE

3 Beds 4 Baths 3,080 SqFt Residential MLS® # 1213985
1201 Neck Rd, PONTE VEDRA BEACH

$1,199,000

↓ $800,000

1201 Neck Rd, PONTE VEDRA BEACH

4 Beds 3 Baths 2,611 SqFt Residential MLS® # 1213962