diff --git a/internal/daemon/controller/handler.go b/internal/daemon/controller/handler.go
index e3ef12657..5f4affc50 100644
--- a/internal/daemon/controller/handler.go
+++ b/internal/daemon/controller/handler.go
@@ -6,6 +6,8 @@ package controller
 import (
 	"bytes"
 	"context"
+	"crypto/rand"
+	"encoding/base64"
 	"encoding/json"
 	"errors"
 	"fmt"
@@ -98,7 +100,8 @@ func (c *Controller) apiHandler(props HandlerProperties) (http.Handler, error) {
 		return nil, err
 	}
 
-	corsWrappedHandler := wrapHandlerWithCors(mux, props)
+	cspWrappedHandler := wrapHandlerWithCsp(mux, props, isUiRequest)
+	corsWrappedHandler := wrapHandlerWithCors(cspWrappedHandler, props)
 	commonWrappedHandler := wrapHandlerWithCommonFuncs(corsWrappedHandler, c, props)
 	callbackInterceptingHandler := wrapHandlerWithCallbackInterceptor(commonWrappedHandler, c)
 	printablePathCheckHandler := cleanhttp.PrintablePathCheckHandler(callbackInterceptingHandler, nil)
@@ -759,3 +762,55 @@ func getActions(urlPath string) []string {
 	// Split the rest on ":", returning all actions and sub-actions
 	return strings.Split(rest, ":")
 }
+
+func wrapHandlerWithCsp(h http.Handler, props HandlerProperties, isUiRequest func(*http.Request) bool) http.Handler {
+	cspKey := "Content-Security-Policy"
+	defaultCsp := ""
+	if headers, ok := props.ListenerConfig.CustomUiResponseHeaders[0]; ok {
+		if vals := headers[cspKey]; len(vals) > 0 {
+			defaultCsp = vals[0]
+		}
+		// Remove CSP from the map so WrapCustomHeadersHandler does not
+		// overwrite the nonce injected value.
+		delete(headers, cspKey)
+	}
+
+	return http.HandlerFunc(func(w http.ResponseWriter, req *http.Request) {
+		if defaultCsp == "" || !isUiRequest(req) {
+			h.ServeHTTP(w, req)
+			return
+		}
+
+		// Static assets get the default CSP without a nonce.
+		if strings.LastIndex(req.URL.Path, ".") != -1 {
+			w.Header().Set(cspKey, defaultCsp)
+			h.ServeHTTP(w, req)
+			return
+		}
+
+		// Generate nonce.
+		b := make([]byte, 16)
+		if _, err := rand.Read(b); err != nil {
+			w.Header().Set(cspKey, defaultCsp)
+			h.ServeHTTP(w, req)
+			return
+		}
+		nonce := base64.StdEncoding.EncodeToString(b)
+
+		// Inject nonce into the style-src directive of the CSP.
+		nonceToken := fmt.Sprintf("'nonce-%s'", nonce)
+
+		csp := defaultCsp
+
+		if strings.Contains(csp, "style-src ") {
+			csp = strings.Replace(csp, "style-src ", fmt.Sprintf("style-src %s ", nonceToken), 1)
+		} else {
+			csp = fmt.Sprintf("%s; style-src %s 'self'", csp, nonceToken)
+		}
+
+		w.Header().Set(cspKey, csp)
+		// Creating a custom key so we can pull it when serving UI page
+		w.Header().Set("X-Boundary-Csp-Nonce", nonce)
+		h.ServeHTTP(w, req)
+	})
+}
diff --git a/internal/daemon/controller/handler_test.go b/internal/daemon/controller/handler_test.go
index ab133fbfe..18dca67f3 100644
--- a/internal/daemon/controller/handler_test.go
+++ b/internal/daemon/controller/handler_test.go
@@ -12,6 +12,7 @@ import (
 	"io"
 	"net"
 	"net/http"
+	"net/http/httptest"
 	"net/url"
 	"strings"
 	"testing"
@@ -19,6 +20,7 @@ import (
 	"github.com/grpc-ecosystem/grpc-gateway/v2/runtime"
 	"github.com/hashicorp/boundary/internal/daemon/controller/handlers"
 	"github.com/hashicorp/boundary/internal/errors"
+	"github.com/hashicorp/go-secure-stdlib/listenerutil"
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 	"google.golang.org/genproto/googleapis/api/httpbody"
@@ -467,3 +469,98 @@ func TestGetActions(t *testing.T) {
 		})
 	}
 }
+
+func TestWrapHandlerWithCsp(t *testing.T) {
+	defaultCsp := "default-src 'none'; script-src 'self' 'wasm-unsafe-eval'; frame-src 'self'; font-src 'self'; connect-src 'self'; img-src 'self' data:; style-src 'self'; media-src 'self'; manifest-src 'self'; style-src-attr 'self'; frame-ancestors 'self'"
+
+	newProps := func(csp string) HandlerProperties {
+		if csp == "" {
+			csp = defaultCsp
+		}
+		headers := http.Header{}
+		headers.Set("Content-Security-Policy", csp)
+		return HandlerProperties{
+			ListenerConfig: &listenerutil.ListenerConfig{
+				CustomUiResponseHeaders: map[int]http.Header{
+					0: headers,
+				},
+			},
+		}
+	}
+
+	inner := http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		w.WriteHeader(http.StatusOK)
+	})
+
+	testCases := []struct {
+		name           string
+		path           string
+		isUi           bool
+		customCsp      string
+		wantNonce      bool
+		wantDefaultCsp bool
+		wantContains   []string
+	}{
+		{
+			name:      "document request gets nonce",
+			path:      "/",
+			isUi:      true,
+			wantNonce: true,
+		},
+		{
+			name:           "static asset gets default CSP without nonce",
+			path:           "/assets/app.js",
+			isUi:           true,
+			wantDefaultCsp: true,
+			wantNonce:      false,
+		},
+		{
+			name:      "non UI request gets no CSP header",
+			path:      "/",
+			isUi:      false,
+			wantNonce: false,
+		},
+		{
+			name:         "custom CSP without style-src gets style-src created",
+			path:         "/",
+			isUi:         true,
+			customCsp:    "default-src 'none'; script-src 'self'",
+			wantContains: []string{"default-src 'none'", "script-src 'self'", "; style-src 'nonce-", "'self'"},
+		},
+	}
+
+	for _, tc := range testCases {
+		t.Run(tc.name, func(t *testing.T) {
+			require := require.New(t)
+			assert := assert.New(t)
+
+			isUiFunc := func(*http.Request) bool { return tc.isUi }
+			handler := wrapHandlerWithCsp(inner, newProps(tc.customCsp), isUiFunc)
+			req := httptest.NewRequest("GET", tc.path, nil)
+			rec := httptest.NewRecorder()
+			handler.ServeHTTP(rec, req)
+
+			csp := rec.Header().Get("Content-Security-Policy")
+
+			if len(tc.wantContains) > 0 {
+				require.NotEmpty(csp)
+				for _, want := range tc.wantContains {
+					assert.Contains(csp, want)
+				}
+				return
+			}
+
+			switch {
+			case tc.wantNonce:
+				require.NotEmpty(csp)
+				assert.Contains(csp, "'nonce-")
+			case tc.wantDefaultCsp:
+				require.NotEmpty(csp)
+				assert.NotContains(csp, "'nonce-")
+				require.Equal(defaultCsp, csp)
+			default:
+				require.Empty(csp)
+			}
+		})
+	}
+}
diff --git a/internal/daemon/controller/handler_ui.go b/internal/daemon/controller/handler_ui.go
index 5f821f16d..e4ec1e9d7 100644
--- a/internal/daemon/controller/handler_ui.go
+++ b/internal/daemon/controller/handler_ui.go
@@ -6,6 +6,7 @@
 package controller
 
 import (
+	"bytes"
 	"context"
 	"net/http"
 	"strings"
@@ -35,6 +36,41 @@ var serveGrantSchema = func(ctx context.Context, w http.ResponseWriter) {
 	w.Write(data)
 }
 
+const cspPlaceholder = "__BOUNDARY_CSP_NONCE__"
+
+// cspWriter wraps an http.ResponseWriter to replace the CSP nonce placeholder
+// in index.html with the actual nonce value.
+type cspWriter struct {
+	http.ResponseWriter
+	nonce string
+	done  bool
+}
+
+// WriteHeader removes the stale Content-Length since the body replacement
+// changes the size.
+func (w *cspWriter) WriteHeader(statusCode int) {
+	// We need to force recalculation to avoid content length mismatch
+	w.ResponseWriter.Header().Del("Content-Length")
+	w.ResponseWriter.WriteHeader(statusCode)
+}
+
+func (w *cspWriter) Write(b []byte) (int, error) {
+	originalLen := len(b)
+	if !w.done {
+		w.done = true
+		b = bytes.Replace(b, []byte(cspPlaceholder), []byte(w.nonce), 1)
+	}
+	_, err := w.ResponseWriter.Write(b)
+	if err != nil {
+		return 0, err
+	}
+	// We return the original length to maintain the io.Writer contract.
+	// Per io.Writer: "Write must return a non-nil error if it returns n < len(p)."
+	// Since we successfully consumed all input bytes, we must return len(p) with nil error.
+	// Returning the modified length would violate this and break the caller's buffer tracking.
+	return originalLen, nil
+}
+
 func handleUiWithAssets(c *Controller) http.Handler {
 	var nextHandler http.Handler
 	if c.conf.RawConfig.DevUiPassthroughDir != "" {
@@ -45,6 +81,8 @@ func handleUiWithAssets(c *Controller) http.Handler {
 
 	return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 		if r.Method != http.MethodGet {
+			// Lets remove nonce in case we return here
+			w.Header().Del("X-Boundary-Csp-Nonce")
 			w.WriteHeader(http.StatusMethodNotAllowed)
 			return
 		}
@@ -80,7 +118,18 @@ func handleUiWithAssets(c *Controller) http.Handler {
 			}
 		}
 
-		// Fall through to the next handler
+		// For document requests, replace the CSP placeholder inside <head>.
+		if r.URL.Path == "/" {
+			if nonce := w.Header().Get("X-Boundary-Csp-Nonce"); nonce != "" {
+				// Remove nonce once we have injected it in the Write() call
+				w.Header().Del("X-Boundary-Csp-Nonce")
+				nextHandler.ServeHTTP(&cspWriter{ResponseWriter: w, nonce: nonce}, r)
+				return
+			}
+		}
+
+		// Strip internal nonce header for non document requests
+		w.Header().Del("X-Boundary-Csp-Nonce")
 		nextHandler.ServeHTTP(w, r)
 	})
 }
diff --git a/internal/daemon/controller/handler_ui_test.go b/internal/daemon/controller/handler_ui_test.go
index 929af249a..e966c8423 100644
--- a/internal/daemon/controller/handler_ui_test.go
+++ b/internal/daemon/controller/handler_ui_test.go
@@ -10,6 +10,7 @@ import (
 	"fmt"
 	"io/ioutil"
 	"net/http"
+	"net/http/httptest"
 	"os"
 	"path/filepath"
 	"testing"
@@ -18,6 +19,41 @@ import (
 	"github.com/stretchr/testify/require"
 )
 
+func TestCspWriter_Write(t *testing.T) {
+	cases := []struct {
+		name     string
+		input    string
+		nonce    string
+		wantBody string
+	}{
+		{
+			name:     "replaces placeholder with nonce",
+			input:    "foo __BOUNDARY_CSP_NONCE__ bar",
+			nonce:    "'nonce-abc123'",
+			wantBody: "foo 'nonce-abc123' bar",
+		},
+		{
+			name:     "no placeholder returns original unchanged",
+			input:    "no placeholder here",
+			nonce:    "'nonce-abc123'",
+			wantBody: "no placeholder here",
+		},
+	}
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			rec := httptest.NewRecorder()
+			w := &cspWriter{
+				ResponseWriter: rec,
+				nonce:          tc.nonce,
+			}
+			n, err := w.Write([]byte(tc.input))
+			require.NoError(t, err)
+			assert.Equal(t, len(tc.input), n, "must return original input length to conform to the io.Writer contract")
+			assert.Equal(t, tc.wantBody, rec.Body.String())
+		})
+	}
+}
+
 func TestUiRouting(t *testing.T) {
 	// Create a temporary directory
 	tempDir, err := ioutil.TempDir("", "boundary-test-")