diff --git a/internal/middleware/extraheaders.go b/internal/middleware/extraheaders.go
index f584633fe..cd207a9f1 100644
--- a/internal/middleware/extraheaders.go
+++ b/internal/middleware/extraheaders.go
@@ -20,17 +20,17 @@
 import (
 	"codeberg.org/gruf/go-debug"
 	"github.com/gin-gonic/gin"
+	"github.com/superseriousbusiness/gotosocial/internal/config"
 )
 
 // ExtraHeaders returns a new gin middleware which adds various extra headers to the response.
 func ExtraHeaders() gin.HandlerFunc {
-	policy := "default-src 'self'"
-	if debug.DEBUG {
-		policy += " localhost:*"
-	}
+	csp := BuildContentSecurityPolicy()
+
 	return func(c *gin.Context) {
 		// Inform all callers which server implementation this is.
 		c.Header("Server", "gotosocial")
+
 		// Prevent google chrome cohort tracking. Originally this was referred
 		// to as FlocBlock. Floc was replaced by Topics in 2022 and the spec says
 		// that interest-cohort will also block Topics (as of 2022-Nov).
@@ -39,7 +39,55 @@ func ExtraHeaders() gin.HandlerFunc {
 		//
 		// See: https://github.com/patcg-individual-drafts/topics
 		c.Header("Permissions-Policy", "browsing-topics=()")
-		// Inform the browser we only load CSS/JS/media from the same domain
-		c.Header("Content-Security-Policy", policy)
+
+		// Inform the browser we only load
+		// CSS/JS/media using the given policy.
+		c.Header("Content-Security-Policy", csp)
 	}
 }
+
+func BuildContentSecurityPolicy() string {
+	// Start with restrictive policy.
+	policy := "default-src 'self'"
+
+	if debug.DEBUG {
+		// Debug is enabled, allow
+		// serving things from localhost
+		// as well (regardless of port).
+		policy += " localhost:*"
+	}
+
+	s3Endpoint := config.GetStorageS3Endpoint()
+	if s3Endpoint == "" {
+		// S3 not configured,
+		// default policy is OK.
+		return policy
+	}
+
+	if config.GetStorageS3Proxy() {
+		// S3 is configured in proxy
+		// mode, default policy is OK.
+		return policy
+	}
+
+	// S3 is on and in non-proxy mode, so we need to add the S3 host to
+	// the policy to allow images and video to be pulled from there too.
+
+	// If secure is false,
+	// use 'http' scheme.
+	scheme := "https"
+	if !config.GetStorageS3UseSSL() {
+		scheme = "http"
+	}
+
+	// Construct endpoint URL.
+	s3EndpointURLStr := scheme + "://" + s3Endpoint
+
+	// https://developer.mozilla.org/en-US/docs/Web/HTTP/Headers/Content-Security-Policy/img-src
+	policy += "; image-src " + s3EndpointURLStr
+
+	// https://developer.mozilla.org/en-US/docs/Web/HTTP/Headers/Content-Security-Policy/media-src
+	policy += "; media-src " + s3EndpointURLStr
+
+	return policy
+}
diff --git a/internal/middleware/middleware_test.go b/internal/middleware/middleware_test.go
new file mode 100644
index 000000000..fecae5dd1
--- /dev/null
+++ b/internal/middleware/middleware_test.go
@@ -0,0 +1,102 @@
+// GoToSocial
+// Copyright (C) GoToSocial Authors admin@gotosocial.org
+// SPDX-License-Identifier: AGPL-3.0-or-later
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package middleware_test
+
+import (
+	"testing"
+
+	"github.com/superseriousbusiness/gotosocial/internal/config"
+	"github.com/superseriousbusiness/gotosocial/internal/middleware"
+)
+
+func TestBuildContentSecurityPolicy(t *testing.T) {
+	type cspTest struct {
+		s3Endpoint string
+		s3Proxy    bool
+		s3Secure   bool
+		expected   string
+		actual     string
+	}
+
+	for _, test := range []cspTest{
+		{
+			s3Endpoint: "",
+			s3Proxy:    false,
+			s3Secure:   false,
+			expected:   "default-src 'self'",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com",
+			s3Proxy:    false,
+			s3Secure:   true,
+			expected:   "default-src 'self'; image-src https://some-bucket-provider.com; media-src https://some-bucket-provider.com",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com:6969",
+			s3Proxy:    false,
+			s3Secure:   true,
+			expected:   "default-src 'self'; image-src https://some-bucket-provider.com:6969; media-src https://some-bucket-provider.com:6969",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com:6969",
+			s3Proxy:    false,
+			s3Secure:   false,
+			expected:   "default-src 'self'; image-src http://some-bucket-provider.com:6969; media-src http://some-bucket-provider.com:6969",
+		},
+		{
+			s3Endpoint: "s3.nl-ams.scw.cloud",
+			s3Proxy:    false,
+			s3Secure:   true,
+			expected:   "default-src 'self'; image-src https://s3.nl-ams.scw.cloud; media-src https://s3.nl-ams.scw.cloud",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com",
+			s3Proxy:    true,
+			s3Secure:   true,
+			expected:   "default-src 'self'",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com:6969",
+			s3Proxy:    true,
+			s3Secure:   true,
+			expected:   "default-src 'self'",
+		},
+		{
+			s3Endpoint: "some-bucket-provider.com:6969",
+			s3Proxy:    true,
+			s3Secure:   true,
+			expected:   "default-src 'self'",
+		},
+		{
+			s3Endpoint: "s3.nl-ams.scw.cloud",
+			s3Proxy:    true,
+			s3Secure:   true,
+			expected:   "default-src 'self'",
+		},
+	} {
+		config.SetStorageS3Endpoint(test.s3Endpoint)
+		config.SetStorageS3Proxy(test.s3Proxy)
+		config.SetStorageS3UseSSL(test.s3Secure)
+
+		csp := middleware.BuildContentSecurityPolicy()
+		if csp != test.expected {
+			t.Logf("expected '%s', got '%s'", test.expected, csp)
+			t.Fail()
+		}
+	}
+}