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    Destin, FL Office Properties & Spaces for Sale

    20 results
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    Renovated Destin Office Space
    $329,800

    Renovated Destin Office Space

    415 Mountain Dr, Destin, FL 32541

    Two renovated office spaces in Destin, Florida, for the price of one.

    • Two renovated office spaces for the price of one – occupy, lease, or do both for ultimate flexibility.
    • Existing lease in place generates $800/month income.
    • Low CAM fees of just $1044 per year.
    • Newly renovated with LVP and marble flooring, fresh paint, and two renovated bathrooms (one with custom shower).
    • Large 1809 sq ft floor plan features a reception area, 4 offices, conference room, file room, and sauna.
    Updated: Aug 15, 2025
    View details
    Destin Office Building with Credit
    $1,425,000

    Destin Office Building with Credit

    135 Benning Dr, Destin, FL 32541

    Large, centrally located Destin property with renovation credit.

    • $100,000 seller credit for renovations.
    • Large property offering a customizable interior layout.
    • Centrally located in Destin with high visibility.
    • Located along the planned Legion Drive extension.
    • Two parking lots and three curb cuts.
    Updated: Apr 29, 2025
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    Destin Office Suite - Harbor Blvd
    $217,000
    746 SF

    Destin Office Suite - Harbor Blvd

    Prime Destin office, 746 sq ft, immediate occupancy.

    543 Harbor Blvd, Destin, FL 32541
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    Destin Office Condo: Prime Location
    $387,500
    1,550 SF

    Destin Office Condo: Prime Location

    1,550 SF Office Suite, Net Lease, Strong Cash Flow

    543 Harbor Blvd, Destin, FL 32541
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    Destin West End Office Space
    $817,500
    4,314 SF

    Destin West End Office Space

    Prime Destin Office: 4,029 SF, For Sale

    150 Azalea Dr, Destin, FL 32541
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    Destin Office Building: Prime Location
    $3,200,000
    11,340 SF

    Destin Office Building: Prime Location

    Class A, three-story office building; excellent visibility.

    4608 Opa Locka Ln, Destin, FL 32541
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    Destin Commercial Building For Sale
    $2,995,000
    13,396 SF

    Destin Commercial Building For Sale

    Prime Destin location, 9,350 SF office space, ample parking.

    35000 Emerald Coast Pkwy, Destin, FL 32541
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    Destin Office Condo - $289K
    $289,000
    880 SF

    Destin Office Condo - $289K

    880 sq ft Office Condo, Great Location

    1221 Airport Rd, Destin, FL 32541
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    Destin Executive Office Building
    $4,950,000
    22,676 SF

    Destin Executive Office Building

    Class A Office, Multi-Tenant, High ROI

    4458 Legendary Dr, Destin, FL 32541
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    Single-Story Office Building on Harbor
    $850,000

    Single-Story Office Building on Harbor

    Single-story office building with front and rear parking.

    727 Harbor Blvd, Destin, FL 32541
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    Destin Office or Retail Space
    $279,000

    Destin Office or Retail Space

    Office or retail space in mixed-use Destin office park.

    114 Palmetto St, Destin, FL 32541
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    Versatile Office and Warehouse Space
    $465,000

    Versatile Office and Warehouse Space

    2,425 SF office/warehouse with high visibility near Destin.

    4014 W Cmns Dr, Destin, FL 32541
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    Class A Office Building
    $4,995,000

    Class A Office Building

    Class A office building in Destin's Regatta Commons.

    4458 Legendary Dr, Destin, FL 32541
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    Class A Office Building
    $4,950,000
    22,676 SF

    Class A Office Building

    Premier office building in Destin's Regatta Commons.

    Legendary Dr, Destin, FL 32541
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    East Destin Office Space
    $465,000
    2,300 SF

    East Destin Office Space

    Nicely appointed office space in a mixed-use condo.

    4507 Furling Ln, Destin, FL 32541
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    Destin Office Suite For Sale
    $299,900

    Destin Office Suite For Sale

    Ground-floor office suite in Diamond Lakes Office Park.

    3997 W Cmns Dr, Destin, FL 32541
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    Destin Office Suite for Sale
    $299,900
    1,260 SF

    Destin Office Suite for Sale

    Professional office suite in Destin, suitable for various uses.

    3997 Commons Dr W, Destin, FL 32541
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    Harbor Blvd Commercial Office Buildings
    $1,950,000
    5,258 SF

    Harbor Blvd Commercial Office Buildings

    Two office buildings on 0.46 acres with parking.

    725 Harbor Blvd, Destin, FL 32541
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    Destin Class A Office Building
    $4,224,000

    Destin Class A Office Building

    Fully leased Class A office building in the heart of Destin.

    4635 Gulfstarr Dr, Destin, FL 32541
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    First Floor Office Suite
    $217,000
    746 SF

    First Floor Office Suite

    Office suite featuring a lobby, break area, and offices.

    543 Harbor Blvd, Destin, FL 32541
    View details
    Based on your search, we've compiled Potential Opportunities for your consideration. Besides 20 Active Listings in Destin, FL, we suggest to view alternatives - similar 60 Off-Market properties to explore as potential leads.

    Explore Off-Market Properties in Destin, FL

    Consider similar Off-Market properties in Destin, FL. You may contact the owners directly to inquire about their potential intentions to sell. To help you make a strong first impression, we can assist by reaching out to these owners with compelling proposals created using our AI tool.

    543 Us-98

    543 Us-98

    Office Properties & Spaces • 5,687 SF
    Value Estimation by Request
    543 Us-98, Destin, FL 32541
    View details
    1221 Airport Rd

    1221 Airport Rd

    Office Properties & Spaces • 880 SF
    Value Estimation by Request
    1221 Airport Rd, Destin, FL 32541
    View details
    4477 Legendary Dr

    4477 Legendary Dr

    Office Properties & Spaces • 10,000 SF
    Value Estimation by Request
    4477 Legendary Dr, Destin, FL 32541
    View details
    1221 Airport Rd Rd

    1221 Airport Rd Rd

    Office Properties & Spaces
    Value Estimation by Request
    1221 Airport Rd Rd, Destin, FL 32541
    View details

    Destin, FL Office Properties & Spaces Investment Opportunities Market Analysis

    Explore 80 office properties & spaces for sale in Destin, FL, showcased through 20 active listings on our real estate platform. These investment opportunities span a total of 8,188,739,194 square feet of properties for sale, with an estimated market value of $18,696,000.

    Prices for office spaces in Destin, FL start at $145,000, averaging $667,714, and reaching up to $3,200,000 — offering options for a variety of budgets and business needs. Daily updated analytics ensure you have the most current data.

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    Browse Office Properties & Spaces for Sale Near Destin, FL

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    Most Searched ZIP Codes in Destin, FL

    • 32541
    • 32550

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