diff --git a/server/routes.go b/server/routes.go
index 67eae34c67..7b25b09c04 100644
--- a/server/routes.go
+++ b/server/routes.go
@@ -403,12 +403,11 @@ func (s *Server) GenerateHandler(c *gin.Context) {
 				msgs = append(msgs, m.Messages...)
 			}
 
+			userMsg := api.Message{Role: "user", Content: req.Prompt}
 			for _, i := range images {
-				imgPrompt := ""
-				msgs = append(msgs, api.Message{Role: "user", Content: fmt.Sprintf("[img-%d]"+imgPrompt, i.ID)})
+				userMsg.Images = append(userMsg.Images, i.Data)
 			}
-
-			values.Messages = append(msgs, api.Message{Role: "user", Content: req.Prompt})
+			values.Messages = append(msgs, userMsg)
 		}
 
 		values.Think = req.Think != nil && req.Think.Bool()
@@ -429,12 +428,31 @@ func (s *Server) GenerateHandler(c *gin.Context) {
 			b.WriteString(s)
 		}
 
-		if err := tmpl.Execute(&b, values); err != nil {
-			c.JSON(http.StatusInternalServerError, gin.H{"error": err.Error()})
-			return
-		}
+		// check that we're in the `api/chat`-like flow, and if so, generate the
+		// prompt the same way
+		// TEMP(drifkin): we should really just detect the chat-like flow and call
+		// the real chat handler, but doing this as a stopgap to get renderer
+		// support for generate
+		if values.Messages != nil && values.Suffix == "" && req.Template == "" {
+			prompt, images, err = chatPrompt(c.Request.Context(), m, r.Tokenize, opts, values.Messages, []api.Tool{}, req.Think)
+			if err != nil {
+				c.JSON(http.StatusInternalServerError, gin.H{"error": err.Error()})
+				return
+			}
+			// TEMP(drifkin): req.Context will be removed very soon, but we're temporarily supporting it in this flow here
+			if req.Context != nil {
+				b.WriteString(prompt)
+				prompt = b.String()
+			}
+		} else {
+			// legacy flow
+			if err := tmpl.Execute(&b, values); err != nil {
+				c.JSON(http.StatusInternalServerError, gin.H{"error": err.Error()})
+				return
+			}
 
-		prompt = b.String()
+			prompt = b.String()
+		}
 	}
 
 	// If debug mode is enabled, return the rendered template instead of calling the model
diff --git a/server/routes_debug_test.go b/server/routes_debug_test.go
index cc35221090..c27afdb4a4 100644
--- a/server/routes_debug_test.go
+++ b/server/routes_debug_test.go
@@ -146,7 +146,7 @@ func TestGenerateDebugRenderOnly(t *testing.T) {
 				DebugRenderOnly: true,
 			},
 			expectDebug:     true,
-			expectTemplate:  "[img-0]\n\nDescribe this image",
+			expectTemplate:  "[img-0]Describe this image",
 			expectNumImages: 1,
 		},
 		{
diff --git a/server/routes_generate_renderer_test.go b/server/routes_generate_renderer_test.go
new file mode 100644
index 0000000000..b280228630
--- /dev/null
+++ b/server/routes_generate_renderer_test.go
@@ -0,0 +1,313 @@
+package server
+
+import (
+	"bytes"
+	"encoding/json"
+	"net/http"
+	"strings"
+	"testing"
+	"time"
+
+	"github.com/gin-gonic/gin"
+	"github.com/google/go-cmp/cmp"
+
+	"github.com/ollama/ollama/api"
+	"github.com/ollama/ollama/discover"
+	"github.com/ollama/ollama/fs/ggml"
+	"github.com/ollama/ollama/llm"
+)
+
+// TestGenerateWithBuiltinRenderer tests that api/generate uses built-in renderers
+// when in chat-like flow (messages present, no suffix, no template)
+func TestGenerateWithBuiltinRenderer(t *testing.T) {
+	gin.SetMode(gin.TestMode)
+
+	mock := mockRunner{
+		CompletionResponse: llm.CompletionResponse{
+			Done:               true,
+			DoneReason:         llm.DoneReasonStop,
+			PromptEvalCount:    1,
+			PromptEvalDuration: 1,
+			EvalCount:          1,
+			EvalDuration:       1,
+		},
+	}
+
+	s := Server{
+		sched: &Scheduler{
+			pendingReqCh:  make(chan *LlmRequest, 1),
+			finishedReqCh: make(chan *LlmRequest, 1),
+			expiredCh:     make(chan *runnerRef, 1),
+			unloadedCh:    make(chan any, 1),
+			loaded:        make(map[string]*runnerRef),
+			newServerFn:   newMockServer(&mock),
+			getGpuFn:      getGpuFn,
+			getCpuFn:      getCpuFn,
+			reschedDelay:  250 * time.Millisecond,
+			loadFn: func(req *LlmRequest, _ *ggml.GGML, _ discover.GpuInfoList, _ bool) bool {
+				time.Sleep(time.Millisecond)
+				req.successCh <- &runnerRef{
+					llama: &mock,
+				}
+				return false
+			},
+		},
+	}
+
+	go s.sched.Run(t.Context())
+
+	// Create a model with a built-in renderer (qwen3-coder)
+	_, digest := createBinFile(t, ggml.KV{
+		"general.architecture":          "qwen3",
+		"qwen3.block_count":             uint32(1),
+		"qwen3.context_length":          uint32(8192),
+		"qwen3.embedding_length":        uint32(4096),
+		"qwen3.attention.head_count":    uint32(32),
+		"qwen3.attention.head_count_kv": uint32(8),
+		"tokenizer.ggml.tokens":         []string{""},
+		"tokenizer.ggml.scores":         []float32{0},
+		"tokenizer.ggml.token_type":     []int32{0},
+	}, []*ggml.Tensor{
+		{Name: "token_embd.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_norm.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_down.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_gate.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_up.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_norm.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_k.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_output.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_q.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_v.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "output.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+	})
+
+	// Create a model with the qwen3-coder renderer
+	w := createRequest(t, s.CreateHandler, api.CreateRequest{
+		Model:    "test-renderer",
+		Files:    map[string]string{"file.gguf": digest},
+		Renderer: "qwen3-coder",
+		Stream:   &stream,
+	})
+
+	if w.Code != http.StatusOK {
+		t.Fatalf("expected status 200, got %d", w.Code)
+	}
+
+	mock.CompletionResponse.Content = "Hi!"
+
+	t.Run("chat-like flow uses renderer", func(t *testing.T) {
+		// Test that when using messages (chat-like flow), the built-in renderer is used
+		w := createRequest(t, s.GenerateHandler, api.GenerateRequest{
+			Model:  "test-renderer",
+			Prompt: "Write a hello world function",
+			Stream: &stream,
+		})
+
+		if w.Code != http.StatusOK {
+			t.Errorf("expected status 200, got %d", w.Code)
+		}
+
+		// The qwen3-coder renderer produces output with <|im_start|> and <|im_end|> tags
+		// When messages are built internally from prompt, it should use the renderer
+		if !strings.Contains(mock.CompletionRequest.Prompt, "<|im_start|>") {
+			t.Errorf("expected prompt to contain <|im_start|> from qwen3-coder renderer, got: %s", mock.CompletionRequest.Prompt)
+		}
+
+		if !strings.Contains(mock.CompletionRequest.Prompt, "<|im_end|>") {
+			t.Errorf("expected prompt to contain <|im_end|> from qwen3-coder renderer, got: %s", mock.CompletionRequest.Prompt)
+		}
+	})
+
+	t.Run("chat-like flow with system message uses renderer", func(t *testing.T) {
+		// Test that system messages work with the renderer
+		w := createRequest(t, s.GenerateHandler, api.GenerateRequest{
+			Model:  "test-renderer",
+			Prompt: "Write a hello world function",
+			System: "You are a helpful coding assistant.",
+			Stream: &stream,
+		})
+
+		if w.Code != http.StatusOK {
+			t.Errorf("expected status 200, got %d", w.Code)
+		}
+
+		// Should contain the system message and use renderer format
+		if !strings.Contains(mock.CompletionRequest.Prompt, "<|im_start|>system") {
+			t.Errorf("expected prompt to contain system message with renderer format, got: %s", mock.CompletionRequest.Prompt)
+		}
+
+		if !strings.Contains(mock.CompletionRequest.Prompt, "You are a helpful coding assistant.") {
+			t.Errorf("expected prompt to contain system message content, got: %s", mock.CompletionRequest.Prompt)
+		}
+	})
+
+	t.Run("custom template bypasses renderer", func(t *testing.T) {
+		// Test that providing a custom template uses the legacy flow
+		w := createRequest(t, s.GenerateHandler, api.GenerateRequest{
+			Model:    "test-renderer",
+			Prompt:   "Write a hello world function",
+			Template: "{{ .Prompt }}",
+			Stream:   &stream,
+		})
+
+		if w.Code != http.StatusOK {
+			t.Errorf("expected status 200, got %d", w.Code)
+		}
+
+		// Should NOT use the renderer format when custom template is provided
+		if strings.Contains(mock.CompletionRequest.Prompt, "<|im_start|>") {
+			t.Errorf("expected prompt to NOT use renderer when custom template provided, got: %s", mock.CompletionRequest.Prompt)
+		}
+
+		// Should just be the raw prompt from the template
+		if diff := cmp.Diff(mock.CompletionRequest.Prompt, "Write a hello world function"); diff != "" {
+			t.Errorf("mismatch (-got +want):\n%s", diff)
+		}
+	})
+
+	// Create a model with suffix support for the next test
+	w = createRequest(t, s.CreateHandler, api.CreateRequest{
+		Model: "test-suffix-renderer",
+		From:  "test-renderer",
+		Template: `{{- if .Suffix }}<PRE> {{ .Prompt }} <SUF>{{ .Suffix }} <MID>
+{{- else }}{{ .Prompt }}
+{{- end }}`,
+	})
+
+	if w.Code != http.StatusOK {
+		t.Fatalf("expected status 200, got %d", w.Code)
+	}
+
+	t.Run("suffix bypasses renderer", func(t *testing.T) {
+		// Test that providing a suffix uses the legacy flow
+		w := createRequest(t, s.GenerateHandler, api.GenerateRequest{
+			Model:  "test-suffix-renderer",
+			Prompt: "def add(",
+			Suffix: "    return c",
+		})
+
+		if w.Code != http.StatusOK {
+			t.Errorf("expected status 200, got %d", w.Code)
+		}
+
+		// Should NOT use the renderer format when suffix is provided
+		if strings.Contains(mock.CompletionRequest.Prompt, "<|im_start|>") {
+			t.Errorf("expected prompt to NOT use renderer when suffix provided, got: %s", mock.CompletionRequest.Prompt)
+		}
+
+		// Should use the suffix template format
+		if diff := cmp.Diff(mock.CompletionRequest.Prompt, "<PRE> def add( <SUF>    return c <MID>"); diff != "" {
+			t.Errorf("mismatch (-got +want):\n%s", diff)
+		}
+	})
+}
+
+// TestGenerateWithDebugRenderOnly tests that debug_render_only works with built-in renderers
+func TestGenerateWithDebugRenderOnly(t *testing.T) {
+	gin.SetMode(gin.TestMode)
+
+	mock := mockRunner{
+		CompletionResponse: llm.CompletionResponse{
+			Done:               true,
+			DoneReason:         llm.DoneReasonStop,
+			PromptEvalCount:    1,
+			PromptEvalDuration: 1,
+			EvalCount:          1,
+			EvalDuration:       1,
+		},
+	}
+
+	s := Server{
+		sched: &Scheduler{
+			pendingReqCh:  make(chan *LlmRequest, 1),
+			finishedReqCh: make(chan *LlmRequest, 1),
+			expiredCh:     make(chan *runnerRef, 1),
+			unloadedCh:    make(chan any, 1),
+			loaded:        make(map[string]*runnerRef),
+			newServerFn:   newMockServer(&mock),
+			getGpuFn:      getGpuFn,
+			getCpuFn:      getCpuFn,
+			reschedDelay:  250 * time.Millisecond,
+			loadFn: func(req *LlmRequest, _ *ggml.GGML, _ discover.GpuInfoList, _ bool) bool {
+				time.Sleep(time.Millisecond)
+				req.successCh <- &runnerRef{
+					llama: &mock,
+				}
+				return false
+			},
+		},
+	}
+
+	go s.sched.Run(t.Context())
+
+	// Create a model with a built-in renderer
+	_, digest := createBinFile(t, ggml.KV{
+		"general.architecture":          "qwen3",
+		"qwen3.block_count":             uint32(1),
+		"qwen3.context_length":          uint32(8192),
+		"qwen3.embedding_length":        uint32(4096),
+		"qwen3.attention.head_count":    uint32(32),
+		"qwen3.attention.head_count_kv": uint32(8),
+		"tokenizer.ggml.tokens":         []string{""},
+		"tokenizer.ggml.scores":         []float32{0},
+		"tokenizer.ggml.token_type":     []int32{0},
+	}, []*ggml.Tensor{
+		{Name: "token_embd.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_norm.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_down.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_gate.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_up.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.ffn_norm.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_k.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_output.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_q.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "blk.0.attn_v.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+		{Name: "output.weight", Shape: []uint64{1}, WriterTo: bytes.NewReader(make([]byte, 4))},
+	})
+
+	w := createRequest(t, s.CreateHandler, api.CreateRequest{
+		Model:    "test-debug-renderer",
+		Files:    map[string]string{"file.gguf": digest},
+		Renderer: "qwen3-coder",
+		Stream:   &stream,
+	})
+
+	if w.Code != http.StatusOK {
+		t.Fatalf("expected status 200, got %d", w.Code)
+	}
+
+	t.Run("debug_render_only with renderer", func(t *testing.T) {
+		w := createRequest(t, s.GenerateHandler, api.GenerateRequest{
+			Model:           "test-debug-renderer",
+			Prompt:          "Write a hello world function",
+			System:          "You are a coding assistant",
+			DebugRenderOnly: true,
+		})
+
+		if w.Code != http.StatusOK {
+			t.Errorf("expected status 200, got %d", w.Code)
+		}
+
+		var resp api.GenerateResponse
+		if err := json.NewDecoder(w.Body).Decode(&resp); err != nil {
+			t.Fatal(err)
+		}
+
+		if resp.DebugInfo == nil {
+			t.Fatalf("expected debug info, got nil")
+		}
+
+		// Verify that the rendered template uses the built-in renderer
+		if !strings.Contains(resp.DebugInfo.RenderedTemplate, "<|im_start|>") {
+			t.Errorf("expected rendered template to use qwen3-coder renderer format, got: %s", resp.DebugInfo.RenderedTemplate)
+		}
+
+		if !strings.Contains(resp.DebugInfo.RenderedTemplate, "You are a coding assistant") {
+			t.Errorf("expected rendered template to contain system message, got: %s", resp.DebugInfo.RenderedTemplate)
+		}
+
+		if !strings.Contains(resp.DebugInfo.RenderedTemplate, "Write a hello world function") {
+			t.Errorf("expected rendered template to contain prompt, got: %s", resp.DebugInfo.RenderedTemplate)
+		}
+	})
+}