diff --git a/internal/x402/payer_context_test.go b/internal/x402/payer_context_test.go
new file mode 100644
index 00000000..81b13ccc
--- /dev/null
+++ b/internal/x402/payer_context_test.go
@@ -0,0 +1,160 @@
+package x402
+
+import (
+	"encoding/json"
+	"io"
+	"net/http"
+	"net/http/httptest"
+	"strconv"
+	"strings"
+	"testing"
+)
+
+func TestSplicePayerSystemMessage(t *testing.T) {
+	payer := "0x2447b86f22245fa1271978bF37907D07EDE06261"
+
+	t.Run("prepends system message and preserves the rest", func(t *testing.T) {
+		body := []byte(`{"model":"openrouter/auto","stream":true,"messages":[{"role":"user","content":"claim my airdrop"}]}`)
+		out, ok := splicePayerSystemMessage(body, payer)
+		if !ok {
+			t.Fatalf("expected ok")
+		}
+		var doc struct {
+			Model    string `json:"model"`
+			Stream   bool   `json:"stream"`
+			Messages []struct {
+				Role    string `json:"role"`
+				Content string `json:"content"`
+			} `json:"messages"`
+		}
+		if err := json.Unmarshal(out, &doc); err != nil {
+			t.Fatalf("unmarshal: %v", err)
+		}
+		if doc.Model != "openrouter/auto" || !doc.Stream {
+			t.Fatalf("sibling fields not preserved: %+v", doc)
+		}
+		if len(doc.Messages) != 2 {
+			t.Fatalf("want 2 messages, got %d", len(doc.Messages))
+		}
+		if doc.Messages[0].Role != "system" || !strings.Contains(doc.Messages[0].Content, payer) {
+			t.Fatalf("system payer message not first: %+v", doc.Messages[0])
+		}
+		if doc.Messages[1].Content != "claim my airdrop" {
+			t.Fatalf("user message mangled: %+v", doc.Messages[1])
+		}
+	})
+
+	t.Run("non-JSON body passes through", func(t *testing.T) {
+		body := []byte("not json")
+		out, ok := splicePayerSystemMessage(body, payer)
+		if ok || string(out) != "not json" {
+			t.Fatalf("expected byte-identical passthrough, got ok=%v out=%q", ok, out)
+		}
+	})
+
+	t.Run("JSON without messages passes through", func(t *testing.T) {
+		body := []byte(`{"model":"x"}`)
+		out, ok := splicePayerSystemMessage(body, payer)
+		if ok || string(out) != `{"model":"x"}` {
+			t.Fatalf("expected passthrough, got ok=%v out=%q", ok, out)
+		}
+	})
+}
+
+// proxyBodySeen runs a request through buildUpstreamProxy for the given rule
+// and returns the body + headers the upstream received.
+func proxyBodySeen(t *testing.T, rule *RouteRule, reqPath, body string, hdr map[string]string) (string, http.Header) {
+	t.Helper()
+	var gotBody string
+	var gotHeader http.Header
+	upstream := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		b, _ := io.ReadAll(r.Body)
+		gotBody = string(b)
+		gotHeader = r.Header.Clone()
+		w.WriteHeader(http.StatusOK)
+	}))
+	defer upstream.Close()
+	rule.UpstreamURL = upstream.URL
+
+	proxy, err := buildUpstreamProxy(rule)
+	if err != nil {
+		t.Fatalf("buildUpstreamProxy: %v", err)
+	}
+	req := httptest.NewRequest(http.MethodPost, reqPath, strings.NewReader(body))
+	req.Header.Set("Content-Type", "application/json")
+	for k, v := range hdr {
+		req.Header.Set(k, v)
+	}
+	rec := httptest.NewRecorder()
+	proxy.ServeHTTP(rec, req)
+	if rec.Code != http.StatusOK {
+		t.Fatalf("proxy status = %d", rec.Code)
+	}
+	return gotBody, gotHeader
+}
+
+func TestBuildUpstreamProxy_InjectsPayerContextForAgentOffers(t *testing.T) {
+	payer := "0xD0391EeDc3268F3deeF1F05fff5D7aEf82F64cCF"
+	chatBody := `{"model":"openrouter/auto","messages":[{"role":"user","content":"claim mine"}]}`
+
+	t.Run("agent offer with verified payer gets the system message", func(t *testing.T) {
+		rule := &RouteRule{OfferType: "agent", StripPrefix: "/services/claim-bot"}
+		body, _ := proxyBodySeen(t, rule, "/services/claim-bot/v1/chat/completions", chatBody,
+			map[string]string{HeaderPaymentPayer: payer})
+		if !strings.Contains(body, payer) || !strings.Contains(body, "x402 payment context") {
+			t.Fatalf("payer context not injected; upstream saw: %s", body)
+		}
+		if !strings.Contains(body, "claim mine") {
+			t.Fatalf("original user message lost: %s", body)
+		}
+	})
+
+	t.Run("falls back to SIWX verified wallet", func(t *testing.T) {
+		rule := &RouteRule{OfferType: "agent", StripPrefix: "/services/claim-bot"}
+		body, _ := proxyBodySeen(t, rule, "/services/claim-bot/v1/chat/completions", chatBody,
+			map[string]string{HeaderVerifiedWallet: payer})
+		if !strings.Contains(body, payer) {
+			t.Fatalf("verified-wallet fallback not injected; upstream saw: %s", body)
+		}
+	})
+
+	t.Run("no identity header means untouched body", func(t *testing.T) {
+		rule := &RouteRule{OfferType: "agent", StripPrefix: "/services/claim-bot"}
+		body, _ := proxyBodySeen(t, rule, "/services/claim-bot/v1/chat/completions", chatBody, nil)
+		if body != chatBody {
+			t.Fatalf("body modified without identity header: %s", body)
+		}
+	})
+
+	t.Run("non-agent offers are untouched", func(t *testing.T) {
+		rule := &RouteRule{OfferType: "http", StripPrefix: "/services/api"}
+		body, _ := proxyBodySeen(t, rule, "/services/api/v1/chat/completions", chatBody,
+			map[string]string{HeaderPaymentPayer: payer})
+		if body != chatBody {
+			t.Fatalf("http offer body modified: %s", body)
+		}
+	})
+
+	t.Run("normalized bare path also gets injection", func(t *testing.T) {
+		// Buyers frequently POST to the service base; normalizeChatCompletionsPath
+		// rewrites it to /v1/chat/completions, and injection must follow.
+		rule := &RouteRule{OfferType: "agent", StripPrefix: "/services/claim-bot"}
+		body, _ := proxyBodySeen(t, rule, "/services/claim-bot", chatBody,
+			map[string]string{HeaderPaymentPayer: payer})
+		if !strings.Contains(body, payer) {
+			t.Fatalf("payer context not injected on normalized path; upstream saw: %s", body)
+		}
+	})
+
+	t.Run("content-length is recomputed", func(t *testing.T) {
+		rule := &RouteRule{OfferType: "agent", StripPrefix: "/services/claim-bot"}
+		body, hdr := proxyBodySeen(t, rule, "/services/claim-bot/v1/chat/completions", chatBody,
+			map[string]string{HeaderPaymentPayer: payer})
+		if cl := hdr.Get("Content-Length"); cl != "" {
+			n, err := strconv.Atoi(cl)
+			if err != nil || n != len(body) {
+				t.Fatalf("content-length %q != body length %d", cl, len(body))
+			}
+		}
+	})
+}
diff --git a/internal/x402/verifier.go b/internal/x402/verifier.go
index 02fa2c37..8bda591c 100644
--- a/internal/x402/verifier.go
+++ b/internal/x402/verifier.go
@@ -2,7 +2,10 @@ package x402
 
 import (
 	"bufio"
+	"bytes"
+	"encoding/json"
 	"fmt"
+	"io"
 	"log"
 	"net"
 	"net/http"
@@ -10,6 +13,7 @@ import (
 	"net/url"
 	"os"
 	"sort"
+	"strconv"
 	"strings"
 	"sync/atomic"
 	"time"
@@ -824,6 +828,7 @@ func buildUpstreamProxy(rule *RouteRule) (http.Handler, error) {
 			} else if rule.UpstreamAuth != "" {
 				pr.Out.Header.Set("Authorization", rule.UpstreamAuth)
 			}
+			injectAgentPayerContext(pr, rule)
 		},
 		ErrorHandler: func(w http.ResponseWriter, r *http.Request, err error) {
 			log.Printf("x402-verifier: upstream proxy error for %s/%s: %v", rule.OfferNamespace, rule.OfferName, err)
@@ -837,6 +842,101 @@ func buildUpstreamProxy(rule *RouteRule) (http.Handler, error) {
 // agent upstreams (LiteLLM, Hermes).
 const chatCompletionsPath = "/v1/chat/completions"
 
+// payerContextBodyLimit caps how much of a chat-completions request body the
+// verifier buffers to splice in the payer-context system message. Larger
+// bodies pass through byte-identical.
+const payerContextBodyLimit = 4 << 20
+
+// injectAgentPayerContext rewrites a paid agent-offer chat request so the
+// verified payer wallet rides IN-BAND as a leading system message. The
+// X-Payment-Payer header alone doesn't reach the model — agent runtimes drop
+// HTTP headers before the LLM sees the conversation — so without this a buyer
+// must repeat their own address in the prompt. Identity headers are
+// verifier-set only (client copies are stripped at HandleProxy entry), so the
+// injected value is an authenticated fact.
+//
+// Injection is strictly best-effort: any shape we don't fully understand
+// (non-JSON, no messages array, oversized or unreadable body, compressed
+// content) leaves the request byte-identical rather than risking a paid
+// request.
+func injectAgentPayerContext(pr *httputil.ProxyRequest, rule *RouteRule) {
+	if rule.OfferType != "agent" || pr.Out.Method != http.MethodPost ||
+		pr.Out.URL.Path != chatCompletionsPath || pr.Out.Body == nil {
+		return
+	}
+	if ce := pr.In.Header.Get("Content-Encoding"); ce != "" && !strings.EqualFold(ce, "identity") {
+		return
+	}
+	if ct := pr.In.Header.Get("Content-Type"); ct != "" && !strings.Contains(strings.ToLower(ct), "json") {
+		return
+	}
+	payer := pr.In.Header.Get(HeaderPaymentPayer)
+	if payer == "" {
+		payer = pr.In.Header.Get(HeaderVerifiedWallet)
+	}
+	if payer == "" {
+		return
+	}
+
+	orig := pr.Out.Body
+	body, err := io.ReadAll(io.LimitReader(orig, payerContextBodyLimit+1))
+	if err != nil || len(body) > payerContextBodyLimit {
+		// Splice the consumed bytes back in front of the unread remainder so
+		// the upstream still receives the full original body.
+		pr.Out.Body = struct {
+			io.Reader
+			io.Closer
+		}{io.MultiReader(bytes.NewReader(body), orig), orig}
+		return
+	}
+	orig.Close()
+
+	newBody, ok := splicePayerSystemMessage(body, payer)
+	if !ok {
+		newBody = body
+	}
+	pr.Out.Body = io.NopCloser(bytes.NewReader(newBody))
+	pr.Out.ContentLength = int64(len(newBody))
+	pr.Out.Header.Set("Content-Length", strconv.Itoa(len(newBody)))
+}
+
+// splicePayerSystemMessage prepends a system message carrying the verified
+// payer wallet to an OpenAI chat-completions JSON body. Returns the original
+// bytes and false when the body isn't the expected shape.
+func splicePayerSystemMessage(body []byte, payer string) ([]byte, bool) {
+	var doc map[string]json.RawMessage
+	if err := json.Unmarshal(body, &doc); err != nil {
+		return body, false
+	}
+	rawMsgs, ok := doc["messages"]
+	if !ok {
+		return body, false
+	}
+	var messages []json.RawMessage
+	if err := json.Unmarshal(rawMsgs, &messages); err != nil {
+		return body, false
+	}
+	note, err := json.Marshal(map[string]string{
+		"role": "system",
+		"content": "x402 payment context: this request was paid by wallet " + payer +
+			" (payer identity verified on-chain by the payment gateway; buyers cannot spoof it). " +
+			"When the buyer refers to their own wallet or address without spelling it out, use this address.",
+	})
+	if err != nil {
+		return body, false
+	}
+	merged, err := json.Marshal(append([]json.RawMessage{note}, messages...))
+	if err != nil {
+		return body, false
+	}
+	doc["messages"] = merged
+	newBody, err := json.Marshal(doc)
+	if err != nil {
+		return body, false
+	}
+	return newBody, true
+}
+
 // normalizeChatCompletionsPath forgives the common wrong-path shapes buyers
 // send to chat-completions offers. External x402 clients (and the prompts on
 // older 402 pages) frequently POST to the bare service base or to